BJS, 2021, 108, 1448–1464
2
DOI: 10.1093/bjs/znab336
Advance Access Publication Date: 13 November 2021
Original Article
Death following pulmonary complications of surgery
before and during the SARS-CoV-2 pandemic
*
Correspondence to: James Glasbey, NIHR Global Health Research Unit on Global Surgery, Institute of Translational Medicine, University of Birmingham, Birmingham
B15 2TH, UK (e-mail: j.glasbey@bham.ac.uk; collaborate@starsurg.org )
Abstract
Background: This study aimed to determine the impact of pulmonary complications on death after surgery both before and during
the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic.
Methods: This was a patient-level, comparative analysis of two, international prospective cohort studies: one before the pandemic
(January–October 2019) and the second during the SARS-CoV-2 pandemic (local emergence of COVID-19 up to 19 April 2020). Both included patients undergoing elective resection of an intra-abdominal cancer with curative intent across five surgical oncology
disciplines. Patient selection and rates of 30-day postoperative pulmonary complications were compared. The primary outcome was
30-day postoperative mortality. Mediation analysis using a natural-effects model was used to estimate the proportion of deaths
during the pandemic attributable to SARS-CoV-2 infection.
Results: This study included 7402 patients from 50 countries; 3031 (40.9 per cent) underwent surgery before and 4371 (59.1 per cent)
during the pandemic. Overall, 4.3 per cent (187 of 4371) developed postoperative SARS-CoV-2 in the pandemic cohort. The pulmonary
complication rate was similar (7.1 per cent (216 of 3031) versus 6.3 per cent (274 of 4371); P ¼ 0.158) but the mortality rate was significantly higher (0.7 per cent (20 of 3031) versus 2.0 per cent (87 of 4371); P < 0.001) among patients who had surgery during the pandemic.
The adjusted odds of death were higher during than before the pandemic (odds ratio (OR) 2.72, 95 per cent c.i. 1.58 to 4.67; P < 0.001).
In mediation analysis, 54.8 per cent of excess postoperative deaths during the pandemic were estimated to be attributable to
SARS-CoV-2 (OR 1.73, 1.40 to 2.13; P < 0.001).
Conclusion: Although providers may have selected patients with a lower risk profile for surgery during the pandemic, this did not
mitigate the likelihood of death through SARS-CoV-2 infection. Care providers must act urgently to protect surgical patients from
SARS-CoV-2 infection.
*Members of the STARSurg Collaborative and COVIDSurg Collaborative are co-authors of this article and are listed under the heading Collaborators
Presented to the Association of Surgeons in Training Surgical Summit, October 2020 (virtual, UK), National Research Collaborative Meeting, December 2020 (virtual,
UK), Royal Australasian College of Surgeons Annual Academic Surgery Conference, November 2020 (virtual, Australasia), Sugical Research Society, March 2021,
https://doi.org/10.1093/bjs/znab282.027 (virtual, UK).
Lay summary
This study compared death rates in patients who developed pulmonary complications of surgery before and during the pandemic
in two large, international studies. Patients who underwent surgery during the pandemic tended to be younger and fitter. Overall,
4.3 per cent were diagnosed with SARS-CoV-2 infection after surgery in the pandemic cohort. Deaths within 30 days after surgery
tripled during the first wave of the pandemic (from 0.7 to 2.0 per cent), whereas the rate of pulmonary complications remained the
similar (7.1 to 6.3 per cent). Over half of these excess deaths (54.8 per cent) were estimated to be related to SARS-CoV-2 infection.
Introduction
Pulmonary complications are a common sequelae of abdominal
cancer surgery, with an incidence of around 8 per cent in prospective data sets1–3. Pulmonary sequelae include pneumonia, acute respiratory distress syndrome (ARDS), and/or unexpected ventilation,
linked by a common pathophysiological mechanism of pulmonary
collapse and airway contamination4. Before coronavirus disease
2019 (COVID-19), existing data linked pulmonary complications
with a moderate risk of death and critical care use5,6.
Early in the pandemic, it was recognized that patients faced
an increased risk of death from pulmonary complications if they
became infected with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in the perioperative phase7. To reduce
in-hospital transmission, health providers around the world
Received: May 22, 2021. Revised: August 03, 2021. Accepted: August 29, 2021
C The Author(s) 2021. Published by Oxford University Press on behalf of BJS Society Ltd.
V
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/
licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For
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STARSurg Collaborative and COVIDSurg Collaborative
STARSurg Collaborative and COVIDSurg Collaborative
Methods
This study was a comparative analysis of combined patient-level
data from two, international, multicentre, prospective observational cohort studies. Both collected routine, anonymized data
with no change to clinical care pathways. Confirmation of
appropriate local or national regulatory approval was required
before patient enrolment. This study was performed according to
STROBE reporting guidelines for observational studies17.
Participants and settings
Data from two international cohort studies from collaborative
groups were combined. Definitions of cases, operations, and outcomes were harmonious in both studies, allowing and robust interpretation of the combined study data set. The RECON study18
collected data on consecutive adult patients who underwent major abdominal surgery between 21 January 2019 and 23 March
2019 in the UK and Ireland, and between 22 September 2019
and 19 October 2019 in Australia (prepandemic cohort). The
COVIDSurg cancer study collected data on consecutive adult
patients who underwent cancer surgery with curative intent
from the local emergence of COVID-19 (22 February onwards) up
to an interim censoring date of 19 April 2020 (pandemic cohort)19.
Any centre around the world performing cancer surgery was eligible to enrol patients.
Patients undergoing elective (planned) resection of one of five
intra-abdominal cancer types with curative intent were included
in this combined analysis. Eligible surgical oncology disciplines
were colorectal, oesophagogastric, hepatopancreatobiliary (liver,
pancreatic), urological
(prostate,
bladder,
renal),
and
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gynaecological (uterine, ovarian, cervical) surgery. Participating
centres could contribute data about one or more cancer sites
based on local services and capacity. There was an absolute requirement to include all eligible patients during the study inclusion window. Patients with a confirmed SARS-CoV-2-positive test
or suspected COVID-19 (with no test result available) at the time
of surgery were excluded from the pandemic cohort study.
Outcome measures
The primary outcome was death within 30 days after surgery.
The secondary outcome measures were postoperative pulmonary
complication and SARS-CoV-2 infection rates.
Postoperative pulmonary complications were defined as a composite of three outcomes plausibly associated with SARS-CoV-2 infection: pneumonia, defined according to US Centre for Disease
Control criteria4; ARDS, defined according to Berlin consensus criteria4; and unexpected postoperative ventilation (defined as failure of planned postoperative extubation, or subsequent
requirement for non-invasive ventilation, invasive ventilation, or
extracorporeal membrane oxygenation20). This outcome definition has been used previously in defining complications of surgery
in the context of COVID-19 and major randomized trials11,20,21.
Reflecting variable access to testing around the world during
the early phase of the pandemic, SARS-CoV-2 infection was defined pragmatically. SARS-COV-2 testing was performed according to policy and availability at the participating centre.
The primary method of identification was nasopharyngeal swab
testing with quantitative reverse transcriptase–polymerase chain
reaction (RT–qPCR) used to detect the RNA signature of SARSCoV-2. Where RT–qPCR testing was not available, radiological
and clinical diagnosis with features suggestive of COVID-19 were
accepted within the outcome definition22. Patients who were initially suspected of having COVID-19 using either clinical or radiological methods, and who subsequently received a negative
laboratory test, were classified as uninfected. Patients with unknown SARS-COV-2 infection status were combined with those
who were negative for SARS-COV-2 infection to form a variable
describing whether or not patients had a SARS-COV-2 diagnosis.
In the prepandemic data set, all patients were considered uninfected.
Study procedures and definitions
Data in both studies were collected using a collaborative research
methodology23, engaging clinicians, medical students, and allied
healthcare professionals at sites around the world to collect data
according to prepublished study protocols18,19. Anonymized data
were submitted and stored on secure Research Electronic Data
Capture (REDCap) servers at the University of Birmingham
(Birmingham, UK)24. The data sets were homogenized and combined based on variables that shared a common definition and a
complementary data structure18,19.
Clinically relevant co-variables were selected for the purpose
of adjustment for case mix. Sociodemographic and operative
data recorded included: age, sex, ASA physical status classification, obesity (body mass index (BMI) at least 30 kg/m2), smoking
status, co-morbidities (chronic lung disease, cardiovascular disease, diabetes mellitus), operative approach (open or minimally
invasive), operative incision (thoracoabdominal, upper abdominal, or lower abdominal), and operative complexity (complex
major or intermediate/major according to the British United
Provident Association Schedule of Procedures25). Operative
incision was classified as the highest extent to which the incision
reached; for example, an incision crossing the upper and lower
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postponed many elective operations, and cut diagnostic and
outpatient services8. This had a major collateral impact on those
requiring surgery, including patients with cancer facing long
delays and associated morbidity9,10. Yet in some areas, operations for time-critical conditions such as cancer were continued
even during periods with high community SARS-CoV-2 infection
rates. Now, during pandemic recovery, surgery must be urgently
upscaled to address a growing backlog of elective surgery8.
However, measures to protect patients from infection, including
service reconfiguration to provide COVID-19-free surgical pathways11 and routine preoperative testing12, have major financial,
logistical, and staffing implications. Data are needed to support
shared decision-making and justify investment in protective
measures.
Understanding of the relationship between pulmonary complications and postoperative mortality in the pandemic era
remains incomplete. In an international study12 of patients
infected with SARS-CoV-2 in the perioperative phase, 51.2 per
cent developed a pulmonary complication and 23.8 per cent
died. Pulmonary events accounted for 82.6 per cent of deaths in
infected patients. These rates were higher than any reported before the pandemic, even for the highest-risk patient groups2,3,5.
However, this study has been criticized for a lack of comparison
with uninfected patients, and a risk of selection bias in identifying the most severely affected patients13,14. The effect of the
collateral impact on critical care and support services during
the pandemic on capacity to rescue patients after surgical complications also remains unmeasured15,16.
This study aimed to compare mortality after pulmonary complications before and during the pandemic in two international
cohort studies of patients undergoing planned cancer surgery,
and to explore the mediators of any differences observed.
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BJS, 2021, Vol. 108, No. 12
abdomen was classified as upper abdominal). Patients for whom
the primary outcome (mortality) was missing were excluded
from the analysis.
Statistical analysis
Prepandemic
cohort n = 11591
Results
Some 7402 patients were included in this analysis; 3031 (40.9 per
cent) underwent surgery before and 4371 (59.1 per cent) during
the pandemic (Fig. 1). Overall, the surgical case mix was 45.5 per
cent (3368 patients) colorectal, 8.5 per cent (631) oesophagogastric, 11.5 per cent (852) hepatopancreatobiliary, 19.9 per cent
(1475) gynaecological, and 14.5 per cent (1076) urological cancers.
Some 49.0 per cent of patients (3629) underwent open surgery
and a minimally invasive approach was attempted in 51.0 per
cent (3770).
Pandemic cohort
n = 9171
Not eligible n = 4782
Non-abdominal procedure n = 4260
Ineligible procedure (n = 522)
Not eligible n = 8469
Non-elective procedure n = 4232
Benign pathology n = 4237
Eligible patients
n = 3122
Eligible patients
n = 4389
Incomplete mortality data n = 86
Incomplete mortality data n = 91
Included
n = 3031
Included
n = 4371
Combined cohort of patients
undergoing elective abdominal
cancer surgery n = 7402
Fig. 1 Study flow diagram
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Characteristics and postoperative outcomes of patients who
underwent surgery in the prepandemic and pandemic cohorts
were compared. The phenotype of pulmonary complications, and
investigated differences in each component of the composite
measure were analysed. Continuous data were summarized as
mean(s.d.) or median (i.q.r.) based on visual and statistical evaluation for normality, with testing using appropriate parametric or
non-parametric tests. Categorical data were cross-tabulated, and
differences tested using v2 or Fisher’s exact test.
The overall impact of pulmonary complications and death on
surgical systems before and during the pandemic was estimated
by comparing the fraction of mortality attributable to pulmonary
complications—the population attributable fraction26. In the present context, this can be interpreted as the estimated percentage
of all deaths that would not have occurred if no patients in the
cohort had a pulmonary complication.
The influence of timing of surgery (before pandemic versus
pandemic) and SARS-COV-2 infection on the primary outcome
measure (death) was explored in mediation analysis using a natural-effects model27. A classical approach was used with twoway decomposition of total effect into the effect of the time interval of surgery (direct effect), and the proportion of this effect that
was mediated by SARS-COV-2 infection (indirect effect).
Associations between exposure (timing of surgery) and outcome
(death), and then the mediator (SARS-COV-2 infection) and both
exposure (timing of surgery) and outcome (death) were characterized using logistic regression models. The mediation effect estimate therefore represents the proportion of any difference in
death rates between the prepandemic and pandemic cohorts that
can be explained by SARS-COV-2 infection. Bootstrapping of estimates was performed to provide 95 per cent confidence intervals.
Models were adjusted for all clinically relevant co-variables
described above. To explore the effect of inclusion of different
hospitals and countries in the cohort studies and differences in
operative approach, sensitivity analyses were conducted by including only patients from high-income countries and only open
procedures respectively.
Finally, multivariable, mixed-effects (multilevel) logistic
regression models were constructed to identify factors associated
with mortality. To explore the association between postoperative
pulmonary complications and SARS-CoV-2 infection and death
these were included as the key explanatory variables, grouped
into three categories: no pulmonary complication; pulmonary
complication, no SARS-CoV-2; or pulmonary complication, SARSCoV-2 infection. Again, the model was adjusted for the clinically
relevant co-variables described above, with hospital and country
included as random effects. First-order interactions were investigated, and final model selection was informed by the Akaike information criterion and C-statistic.
For all analyses, the threshold for two-sided statistical significance was set at P < 0050. Effect estimates were summarized as
adjusted odds ratios (ORs) with 95 per cent confidence intervals.
Data were analysed using R 3.6.1 (R Foundation for Statistical
Computing, Vienna, Austria), with packages including tidyverse,
finalfit, medflex, and collaboratoR28.
STARSurg Collaborative and COVIDSurg Collaborative
Comparison of case mix in prepandemic and
pandemic data
Comparison of outcomes in prepandemic and
pandemic data
Despite selection of patients with a lower baseline risk for surgery
during the pandemic, there was no reduction in pulmonary complications (7.1 per cent (216 of 3031) before versus 6.3 per cent
(274 of 4371) during the pandemic; P ¼ 0.158), but the mortality
rate was significantly higher during the pandemic (0.7 per cent
(20 of 3031) and 2.0 per cent (87 of 4371) respectively; P < 0.001).
In the pandemic cohort, 4.3 per cent of patients (187 of 4371)
were found to be positive for SARS-CoV-2 in the postoperative period.
Different phenotypes of pulmonary complications were registered before and during the pandemic (Fig. 2a), with a more severe pattern of disease in the pandemic cohort; ARDS was more
common (0.2 per cent before versus 1.2 per cent during pandemic;
P < 0.001), whereas pneumonia was less common (6.0 versus 4.6
per cent; P ¼ 0.013). Postoperative SARS-CoV-2 infection was
strongly associated with pulmonary complications on multivariable analysis of combined data (OR 24.95, 95 per cent c.i. 16.75 to
37.17; P < 0.001) (Table 2).
Before the pandemic, 11 of 20 patients who died had a pulmonary complication. During the pandemic, 45 of 87 patients who
died had a pulmonary complication, of whom 31 had a SARSCoV-2 infection (Fig. 2b). The population fraction of mortality that
was attributable to pulmonary complications increased from 37.0
(95 per cent c.i. 14.6 to 64.1) per cent before the pandemic to 66.0
(48.6 to 79.3) per cent during the pandemic.
Differences in mortality rates
Having surgery during the pandemic was associated with threefold higher adjusted odds of mortality than expected if these
patients had undergone surgery in the prepandemic period (OR
2.72, 95 per cent c.i. 1.58 to 4.67; P < 0.001) (Fig. 3 and Table S1).
This increase in postoperative mortality was largely explained by
SARS-CoV-2 (OR 1.73, 1.40 to 2.13; P < 0.001), with 54.8 per cent of
excess deaths mediated through SARS-CoV-2 infection (indirect
effect). The direct effect of timing of surgery was not significant
(OR 1.57, 0.91 to 2.73; P ¼ 0.108). This was reproduced in a sensitivity analysis for patients from high-income countries only and
those who underwent only open surgical operations (Table S2).
In the combined data set, pulmonary complications in the
presence SARS-CoV-2 infection had higher odds of death (OR
53.74, 23.33 to 123.80; P < 0.001) than pulmonary complications in
patients without COVID-19 (OR 6.91, 3.71 to 12.89; P < 0.001)
(Table 3). When SARS-COV-2 infection was discounted from the
multilevel model, there was no significant change in the associations observed except for pulmonary complications (OR 13.11,
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Table 1 Sociodemographic and operative differences between
the prepandemic and pandemic cohorts
Age (years)
< 60
60–69
> 70
Sex
F
M
ASA grade
I–II
III–V
Obese (BMI 30 kg/m2)
No
Yes
Smoker
Not current
Current
Chronic lung disease
No
Yes
Cardiovascular disease
No
Yes
Diabetes mellitus
No
Yes
Operative approach
Minimally invasive
Open
Operative site
Lower abdominal
Upper abdominal
Thoracoabdominal
Operative complexity
Intermediate/major
Complex major
Surgical specialty
Lower gastrointestinal
Upper gastrointestinal
Hepatopancreatobiliary
Urology
Gynaecology
Country World Bank
classification
Low and middle income
High income
30-day pulmonary
complication
No
Yes
30-day mortality
No
Yes
SARS-COV-2 diagnosis
No
Yes
Before pandemic
(n ¼ 3031)
Pandemic
(n ¼ 4371)
890 (29.4)
926 (30.6)
1215 (40.1)
1391 (31.8)
1287 (29.4)
1693 (38.7)
1430 (47.2)
1601 (52.8)
2214 (50.7)
2157 (49.3)
1956 (68.9)
883 (31.1)
3005 (69.0)
1347 (31.0)
1823 (68.3)
848 (31.7)
3167 (76.6)
970 (23.4)
2699 (89.0)
332 (11.0)
3962 (90.6)
409 (9.4)
2541 (83.8)
490 (16.2)
3912 (89.5)
459 (10.5)
1804 (59.5)
1227 (40.5)
2238 (51.2)
2133 (48.8)
2586 (85.3)
445 (14.7)
3582 (81.9)
789 (18.1)
1709 (56.4)
1321 (43.6)
2061 (47.2)
2308 (52.8)
2457 (81.1)
451 (14.9)
123 (4.1)
3400 (77.8)
856 (19.6)
115 (2.6)
1970 (65.0)
1061 (35.0)
3124 (71.5)
1247 (28.5)
1180 (38.9)
257 (8.5)
279 (9.2)
719 (23.7)
596 (19.7)
2188 (50.1)
374 (8.6)
573 (13.1)
357 (8.2)
879 (20.1)
0 (0)
3031 (100)
541 (12.4)
3830 (87.6)
2821 (93.1)
216 (7.1)
4097 (93.7)
274 (6.3)
3011 (99.3)
20 (0.7)
4284 (98.0)
87 (2.0)
3031 (100)
0 (0)
4147 (94.9)
187 (4.3)
Values in parentheses are percentages. SARS-COV-2, severe acute respiratory
syndrome coronavirus 2.
7.53 to 22.82; P < 0.001), and discrimination remained consistent
(Table S3). This indicates that death associated with SARS-COV-2
infection was being mediated through pulmonary complications.
Discussion
This study compared mortality after pulmonary complications
following elective cancer surgery both before and during the
SARS-CoV-2 pandemic, and postulated mechanisms underlying
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There were differences between patient groups who had surgery
before and during the pandemic (Table 1). Patients undergoing
surgery during the pandemic had a lower baseline risk than those
treated during the pandemic across most risk factors. However,
there was a higher proportion of patients undergoing open procedures during than before the pandemic (52.8 and 43.6 per cent respectively). There were some differences in cancer types included
in the two cohorts, with a higher rate of colorectal and lower rate
of urological cancers in the pandemic cohort. All patients in the
prepandemic cohort were from high-income countries. In the
pandemic cohort, 12.4 per cent of patients (541 of 4371) were
from low- and middle-income countries.
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BJS, 2021, Vol. 108, No. 12
a
Phenotype of pulmonary complications
Pandemic
Before pandemic
6
1
22
26
181
12
9
203
11
ARDS
Pneumonia
Unexpected ventilation
Relationship between SARS-CoV-2 infection diagnosis, pulmonary complications, and death
Before pandemic
Pandemic
78
9 11
205
69
9
31
33
14
160
Death
Pulmonary complication
SARS-Cov-2 diagnosis
Fig. 2 Comparison of outcomes across prepandemic and pandemic cohorts
a Phenotype of pulmonary complications and b relationship between severe acute respiratory syndrome coronavirus 2 (SARS-COV-2) infection diagnosis,
pulmonary complications, and death.
Table 2 Multilevel model of association between SARS-COV-2 infection and pulmonary complications in elective abdominal cancer
surgery
Postoperative
SARS-COV-2 diagnosis
No
Yes
Age (years)
< 60
60–69
> 70
Sex
F
M
ASA grade
I–II
III–V
Obese (BMI 30 kg/m2)
No
Yes
Smoker
Not current
Current
Chronic lung disease
No
Yes
Cardiovascular disease
No
Yes
Diabetes mellitus
No
Yes
Operative approach
Minimally invasive
Open
Operative site
Lower abdominal
Upper abdominal
Thoracoabdominal
Operative complexity
Intermediate/aajor
Complex major
30-day postoperative
pulmonary complications
Univariable analysis
Multilevel analysis
Yes
No
Odds ratio*
P
Odds ratio*
P
390 (5.4)
100 (53.5)
6825 (94.6)
87 (46.5)
1.00 (reference)
20.11 (14.84, 27.33)
< 0.001
1.00 (reference)
24.95 (16.75, 37.17)
< 0.001
92 (4.0)
136 (6.1)
262 (9.0)
2189 (96.0)
2077 (93.9)
2646 (91.0)
1.00 (reference)
1.56 (1.19, 2.05)
2.36 (1.85, 3.02)
0.001
< 0.001
1.00 (reference)
1.26 (0.92, 1.74)
1.96 (1.44, 2.66)
0.153
< 0.001
162 (4.4)
328 (8.7)
3482 (95.6)
3430 (91.3)
1.00 (reference)
2.06 (1.70, 2.50)
< 0.001
1.00 (reference)
1.75 (1.38, 2.22)
< 0.001
244 (4.9)
232 (10.4)
4717 (95.1)
1998 (89.6)
1.00 (reference)
2.24 (1.86, 2.71)
< 0.001
1.00 (reference)
1.60 (1.26, 2.04)
< 0.001
314 (6.3)
128 (7.0)
4676 (93.7)
1690 (93.0)
1.00 (reference)
1.13 (0.91, 1.39)
0.268
1.00 (reference)
1.20 (0.93, 1.54)
0.152
418 (6.3)
72 (9.7)
6243 (93.7)
669 (90.3)
1.00 (reference)
1.61 (1.23, 2.08)
< 0.001
1.00 (reference)
1.59 (1.16, 2.19)
0.004
393 (6.1)
97 (10.2)
6060 (93.9)
852 (89.8)
1.00 (reference)
1.76 (1.38, 2.21)
< 0.001
1.00 (reference)
1.47 (1.10, 1.95)
0.009
226 (5.6)
264 (7.9)
3816 (94.4)
3096 (92.1)
1.00 (reference)
1.44 (1.20, 1.73)
< 0.001
1.00 (reference)
1.08 (0.85, 1.38)
0.512
391 (6.3)
99 (8.0)
5777 (93.7)
1135 (92.0)
1.00 (reference)
1.29 (1.02, 1.61)
0.030
1.00 (reference)
0.94 (0.70, 1.25)
0.648
194 (5.1)
296 (8.2)
3576 (94.9)
3333 (91.8)
1.00 (reference)
1.64 (1.36, 1.98)
< 0.001
1.00 (reference)
1.37 (1.09, 1.74)
0.008
295 (5.0)
114 (8.7)
81 (34.0)
5562 (95.0)
1193 (91.3)
157 (66.0)
1.00 (reference)
1.80 (1.43, 2.25)
9.73 (7.24, 13.00)
< 0.001
< 0.001
1.00 (reference)
1.62 (1.14, 2.30)
10.56 (6.74, 16.54)
270 (5.3)
220 (9.5)
4824 (94.7)
2088 (90.5)
1.00 (reference)
1.88 (1.56, 2.26)
< 0.001
1.00 (reference)
0.86 (0.63, 1.19)
Values in parentheses are percentages unless indicated otherwise. *Values in parentheses are 95 per cent confidence intervals. SARS-COV-2, severe acute
respiratory syndrome coronavirus 2. Number in model ¼ 6644, number of groups ¼ 493, Akaike information criterion ¼ 2646.2, C-statistic ¼ 0.852.
0.007
< 0.001
0.360
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b
41
8
5
STARSurg Collaborative and COVIDSurg Collaborative
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Total effect of pandemic time period OR 2.72 (95% c.i.: 1.58 to 4.67; P < 0.001)
Direct effect of pandemic time period
OR 1.57 (95% c.i.: 0.91 to 2.73, P = 0.108)
percentage mediation 45.2%
Time period
of operation
30-day
mortality
Other mediators
(unmeasured)
SAR-COV-2
infection
Patient
demographics
Patient
co-morbidities
Operative factors
Other confounders
(unmeasured)
Exposure:mediator:outcome baseline confounders
Exposure
Mediator
Outcome
Adjusted confounder
Other confounders
(unmeasured)
Mediator:outcome
confounders
Unadjusted confounder
Fig. 3 Multivariable natural-effects model of postoperative death associated with time interval, mediated by SARS-COV-2 infection
OR, odds ratio; SARS-COV-2, severe acute respiratory syndrome coronavirus 2.
the differences. Two cohort studies were combined to allow direct comparison. Despite attempts to maintain safety during the
pandemic by selecting lower-risk patients for surgery, a threefold increase in the adjusted odds of death was noted. This effect
was largely explained by postoperative SARS-CoV-2 infection,
which was associated with a more severe and lethal pattern of
pulmonary events. It is also notable that the rate of pulmonary
complications was similar between time intervals (7.1 per cent
before versus 6.3 per cent during pandemic; P ¼ 0.158). Given that
SARS-COV-2 infection showed a significant association with the
development of postoperative pulmonary complications (Table 2),
this may be in part due to changes in overall case mix, or more
proactive surveillance and prophylaxis of postoperative pulmonary complications in the pandemic cohort. Additional variability
in the adjusted odds of death between periods may be associated
with the collateral impact on hospitals, and a reduction in capacity to rescue. The overall fraction of deaths after surgery attributable to pulmonary complications doubled between the study
periods (from 37.0 to 66.0 per cent). This has major implications
for health systems around the world. To safely upscale surgery
and address growing backlogs, providers must urgently invest in
measures to reduce the risk of SARS-CoV-2 exposure for surgical
patients. Until vaccination has been implemented universally,
avoiding pulmonary complications is the major research and
practice priority in surgery.
The severe phenotype of pulmonary complications of SARSCoV-2 has now been well described in observational data29.
However, there remains a lack of comparative data for the severity of pulmonary complications in infected and uninfected
patients, fuelling debates around the overall impact on surgical
health systems. Reports of low rates of nosocomial infection
have promoted a narrative around minimal overall impact of
SARS-CoV-2 on the safety of elective surgery. The present study
has demonstrated that SARS-CoV-2-associated pulmonary complications are associated with higher odds of death than pulmonary complications in uninfected patients. Although the absolute
proportion of patients with a SARS-CoV-2 infection has been small
(below 5 per cent), it has had a devastating overall effect. During
the pandemic, pulmonary complications have been the major
driver of death in elective surgical patients, implicated in an estimated 70 per cent of all early mortality. This has important policy
implications. Previous data demonstrated that just 20 per cent of
patients undergoing surgery during the first pandemic wave
underwent care in a protected COVID-19-free surgical pathway,
and under 40 per cent underwent routine screening11. Although
this proportion is likely to have increased over time, these data
support the urgent need for hospital-network realignment in providing COVID-19-protected pathways for all patients undergoing
elective surgery. This represents the most important strategy to reduce avoidable deaths until universal vaccination is available.
Death after surgery (accepting caveats) is the third leading
cause of death worldwide30. There have been global concerns
about the safety of surgery during the pandemic because of the
collateral impact on hospital services such as critical care,
Downloaded from https://academic.oup.com/bjs/article/108/12/1448/6420859 by University of Leeds user on 09 December 2021
Indirect effect (mediated by SARS-COV-2)
OR 1.73 (95% c.i. 1.40 to 2.13: P < 0.001);
Percentage mediation 54.8%
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Table 3 Multilevel model of association between pulmonary complications, SARS-COV-2 infection, and 30-day postoperative
mortality in elective abdominal cancer surgery
30-day postoperative mortality
Multilevel analysis
Died
Alive
Odds ratio*
P
Odds ratio*
P
51 (0.7)
25 (6.4)
31 (31.0)
6861 (99.3)
365 (93.6)
69 (69.0)
1.00 (reference)
9.21 (5.56, 14.89)
60.44 (36.24, 99.91)
< 0.001
< 0.001
1.00 (reference)
6.91 (3.71, 12.89)
53.74 (23.33, 123.80)
< 0.001
< 0.001
11 (0.5)
26 (1.2)
70 (2.4)
2270 (99.5)
2187 (98.8)
2838 (97.6)
1.00 (reference)
2.45 (1.24, 5.19)
5.09 (2.81, 10.18)
0.013
< 0.001
1.00 (reference)
2.39 (0.99, 5.78)
3.77 (1.60, 8.86)
0.052
0.002
34 (0.9)
73 (1.9)
3610 (99.1)
3685 (98.1)
1.00 (reference)
2.10 (1.41, 3.20)
< 0.001
1.00 (reference)
1.38 (0.81, 2.34)
0.241
48 (1.0)
59 (2.6)
4913 (99.0)
2171 (97.4)
1.00 (reference)
2.78 (1.90, 4.10)
< 0.001
1.00 (reference)
2.11 (1.23, 3.64)
0.007
73 (1.5)
20 (1.1)
4917 (98.5)
1798 (98.9)
1.00 (reference)
0.75 (0.44, 1.21)
0.255
1.00 (reference)
0.68 (0.37, 1.24)
0.203
92 (1.4)
15 (2.0)
6569 (98.6)
726 (98.0)
1.00 (reference)
1.48 (0.82, 2.48)
0.167
1.00 (reference)
1.40 (0.69, 2.85)
0.353
92 (1.4)
15 (1.6)
6361 (98.6)
934 (98.4)
1.00 (reference)
1.11 (0.62, 1.87)
0.709
1.00 (reference)
0.76 (0.38, 1.54)
0.453
38 (0.9)
69 (2.1)
4004 (99.1)
3291 (97.9)
1.00 (reference)
2.21 (1.49, 3.32)
< 0.001
1.00 (reference)
1.32 (0.77, 2.28)
0.317
73 (1.2)
34 (2.8)
6095 (98.8)
1200 (97.2)
1.00 (reference)
2.37 (1.55, 3.54)
< 0.001
1.00 (reference)
1.94 (1.10, 3.40)
0.021
21 (0.6)
86 (2.4)
3749 (99.4)
3543 (97.6)
1.00 (reference)
4.33 (2.74, 7.18)
< 0.001
1.00 (reference)
5.40 (2.85, 10.25)
66 (1.1)
27 (2.1)
14 (5.9)
5791 (98.9)
1280 (97.9)
224 (94.1)
1.00 (reference)
1.85 (1.16, 2.87)
5.48 (2.92, 9.62)
0.008
< 0.001
1.00 (reference)
0.55 (0.25, 1.23)
1.53 (0.55, 4.31)
0.144
0.416
55 (1.1)
52 (2.3)
5039 (98.9)
2256 (97.7)
1.00 (reference)
2.11 (1.44, 3.10)
< 0.001
1.00 (reference)
1.65 (0.83, 3.31)
0.155
< 0.001
Values in parentheses are percentages unless indicated otherwise. *Values in parentheses are 95 per cent confidence intervals. SARS-COV-2, severe acute
respiratory syndrome coronavirus 2. Number in model ¼ 6644, number of groups ¼ 493, Akaike information criterion ¼ 756.6, C-statistic ¼ 0.961.
diagnostic and interventional radiology, and medical staffing13.
This could reduce health systems’ capacity to rescue in the perioperative setting15. However, there are no existing high-quality
comparative data that have measured this effect to date. The
present data have demonstrated a higher adjusted likelihood of
death for patients undergoing surgery during the pandemic. The
analysis suggests that this was largely mediated by the sequelae
of SARS-CoV-2 infection rather than collateral effects. This may
demonstrate the capacity of included hospitals to compensate
for system-level stress for patients who underwent surgery. It
cannot, however, provide evidence about overall resilience of surgical systems to maintain surgical capacity, nor the impact on
higher-risk patients who may not have undergone surgery and
faced delays9,10.
This study was able to compare case selection and outcomes
of global elective cancer surgery in two large prospective data
sets collected before and during the pandemic. Both cohorts
adopted the same definitions of pulmonary complications and
measured this a primary outcome measure within the original
studies. However, there were several limitations. First, the data
suggest that some patients at higher baseline risk were not offered surgery; it has not been possible to estimate the impact of
delayed treatment on longer-term outcomes for this group.
Second, complete case ascertainment or complete ascertainment
of SARS-COV-2 infection status cannot be ensured, and it is possible that selection bias was introduced. Any unmeasured SARSCOV-2 infections would have likely inflated pulmonary complications and deaths in the comparison group, so would have led to
underestimation of the association between SARS-COV-2 diagnosis and death. However, previous work15 has been validated for
both case ascertainment and data accuracy across a wide range
of settings, and all centres that did not self-report complete-case
inclusion were excluded. Third, it was not possible to collect data
for all possible risk factors implicated in the aetiology of pulmonary complications; for example, the specific chronic respiratory
pathology and all risk factors from validated scoring systems
such as duration of procedure were not included3. Data points selected were chosen to be practical and pragmatic in the context
of frontline clinical practice during a time of severe systemic
stress. Finally, there were differences in the settings in which
data were collected in the two cohort studies; for example, the
prepandemic cohort included data from three high-income countries, compared with 50 mixed-income countries in the pandemic
cohort. Discrepancies in access to care and clinical practice exist
Downloaded from https://academic.oup.com/bjs/article/108/12/1448/6420859 by University of Leeds user on 09 December 2021
30-day pulmonary complication
No
Yes (Non-COVID)
Yes (COVID)
Age (years)
< 60
60–69
> 70
Sex
F
M
ASA grade
I–II
III–V
Obese (BMI 30 kg/m2)
No
Yes
Smoker
Not current
Current
Chronic lung disease
No
Yes
Cardiovascular disease
No
Yes
Diabetes mellitus
No
Yes
Operative approach
Minimally invasive
Open
Operative site
Lower abdominal
Upper abdominal
Thoracoabdominal
Operative complexity
Intermediate/major
Complex major
Univariable analysis
STARSurg Collaborative and COVIDSurg Collaborative
even between high-income countries; however, this study
adopted the same approach to account for these as in previous
similar analyses15,31 . Some 12.4 per cent of patients in the pandemic cohort study were also from a low- or middle-income
country, and hospitals in these settings are known to have significantly higher rates of postoperative morbidity related to inequities in access to care15. However, the primary findings of the
multivariable analyses were robust in a sensitivity analysis including high-income country data only.
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Collaborators
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BJS, 2021, Vol. 108, No. 12
Carroll, C Collins, K Corless, L Finnegan, A Fowler, A Hogan, M
Kerin, A Lowery, P McAnena, K McKevitt, K Nizami, É Ryan, A
Samy, JC Coffey, R Cunningham, M Devine, D Nally, C Peirce, S
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Macron, E Chouillard, Simone B De, J Bettoni, S Dakpé, B
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Pueblo C Sánchez, A Sánchez-Pernaute, Ortega G Sanz, R SanzLopez, A Torres, M Garcés-Albir, F Lopez, J Martı́n-Arévalo, D
Moro-Valdezate, V Pla-Marti, de Heredia J Beltrán, Andrés Asenjo
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B De, Sanz T Gómez, C Jezieniecki, Del Barrio H Nun
Solórzano Aurusa FJ Ortiz, de Diego A Romero, Soriano M Ruiz,
Dı́az J Trujillo, fernandez A Vazquez, P Lora-Cumplido, MV Sosa,
E Gonzalez-Gonzalez, Bravo AM Minaya, de la Fuente N Alonso,
Labat M Cazador, L Cecchini, CA Espinosa, Toscano M Jimenez,
Campillo A López, G Mancebo, P Martorell, M Munarriz, EJ GrauTalens, B Martin-Perez, Buleje JA Benavides, Prats M Carrasco, PV
Fernández, A Fernández-López, Escudero D Garcı́a, Porcel VJ
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~ oz, Ban
~ os PA Parra, Ros E
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~ a, Faraco M Ramirez, M Ruiz-Marı́n, Rodriguez C Sanchez,
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valle E Del, M Fernández, Lominchar P Lozano, L Martı́n,
Valcarcel C Rey, MA Steiner, M Tudela, Ortúzar J Zorrilla, Matas F
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Maher, S Mastoridis, R Mihai, R Piper, S Prabhu, OBF Risk, U
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M Jibreel, E Lenzi, T Saafan, D Sapre, T Sian, N Watson, A
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Theophilou, G Toogood, R Wade, D Ward, C West, S Annamalai,
C Ashmore, A Boddy, T Hossain, A Kourdouli, A Gvaramadze, A
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N Cirocchi, S Kudchadkar, K Patel, J Sagar, S Shaw, R Talwar, M
Abdalla, R Edmondson, O Ismail, D Jones, K Newton, N
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Garrett, M Mehmood, V Ng, R Al-Habsi, GS Divya, B Keeler, B AlSarireh, R Egan, R Harries, A Henry, M Kittur, Z Li, K Parkins, F
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M Louca, P Rozenbroek, E Rozitis, N Agbinya, E Anderson, G Arwi,
I Barry, C Batchelor, T Chong, LY Choo, L Clark, M Daniels, J Goh,
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W Cambridge, LH Chan, F Gaba, Z Khor, JW Les, R Mak, S Moin,
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F Pattinson, M Raja, H Reyhani, A Shahmiri, O Small, U Soni,
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H Maguire, J McMullan, J Nicoletti, S Samuel, MA Unais, N White,
PC Yao, L Yow, R Brady, P Cheekoty, J Cheong, SJHL Chew, R
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Chieng Hin J Ng, Chungath R Renji, A Royston, E Sharrad, R
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STARSurg Collaborative and COVIDSurg Collaborative
Acknowledgements
The COVIDSurg-Cancer study was preregistered in the
ClinicalTrials.gov institutional registry (NCT04384926), whereas
the RECON study was not. The protocols for both projects have
been published.
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Funding
This report was funded through support from the BJS Society
(STARSurg Collaborative), and a National Institute for Health
Research (NIHR) Global Health Research Unit Grant (NIHR
16.136.79) using UK aid from the UK Government to support
global health research; Association of Coloproctology of Great
Britain and Ireland; Bowel & Cancer Research; Bowel Disease
Research Foundation; Association of Upper Gastrointestinal
Surgeons; British Association of Surgical Oncology; British
Gynaecological
Cancer
Society;
European
Society
of
Coloproctology; NIHR Academy; Sarcoma UK; The Urology
Foundation; Vascular Society for Great Britain and Ireland;
Yorkshire Cancer Research. The funders had no role in the study
design, data collection, analysis and interpretation, or writing of
this report. The views expressed are those of the authors and not
necessarily those of the National Health Service, the NIHR, the
BJS Society, or the UK Department of Health and Social Care.
8.
9.
10.
11.
12.
Disclosure. The authors declare no conflict of interest.
13.
Supplementary material
Supplementary material is available at BJS online.
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