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Article

New Challenges in Surgical Approaches for Colorectal Cancer during the COVID-19 Pandemic

by
Dragos Serban
1,2,†,
Geta Vancea
1,3,†,
Catalin Gabriel Smarandache
1,2,†,
Simona Andreea Balasescu
2,
Gabriel Andrei Gangura
1,4,*,
Daniel Ovidiu Costea
5,6,†,
Mihail Silviu Tudosie
1,7,
Corneliu Tudor
2,
Dan Dumitrescu
1,2,
Ana Maria Dascalu
1,†,
Ciprian Tanasescu
8,9 and
Laura Carina Tribus
10,11,†
1
Faculty of Medicine, “Carol Davila” University of Medicine and Pharmacy Bucharest, 020021 Bucharest, Romania
2
Fourth General Surgery Department, Emergency University Hospital Bucharest, 050098 Bucharest, Romania
3
Clinical Hospital of Infectious and Tropical Diseases “Dr. Victor Babes”, 030303 Bucharest, Romania
4
Second General Surgery Department, Emergency University Hospital Bucharest, Splaiul Independentei, nr. 169, 050098 Bucharest, Romania
5
Faculty of Medicine, General Surgery Department, ‘Ovidius’ University Constanta, 900470 Constanta, Romania
6
First Surgery Department, Emergency County Hospital Constanta, 900591 Constanta, Romania
7
ICU II Toxicology, Clinical Emergency Hospital Bucharest, 014461 Bucharest, Romania
8
Faculty of Medicine, “Lucian Blaga” University Sibiu, 550024 Sibiu, Romania
9
Department of Surgery, Sibiu County Clinical Emergency Hospital, 550245 Sibiu, Romania
10
Faculty of Dental Medicine, “Carol Davila” University of Medicine and Pharmacy, 020021 Bucharest, Romania
11
Department of Internal Medicine, Ilfov Emergency Clinic Hospital Bucharest, 022104 Bucharest, Romania
 
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*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Appl. Sci. 2022, 12(11), 5337; https://doi.org/10.3390/app12115337
Submission received: 20 March 2022 / Revised: 16 May 2022 / Accepted: 22 May 2022 / Published: 25 May 2022
(This article belongs to the Special Issue Effect of COVID-19 on Public Health)
Review Reports Versions Notes

Abstract

:
(1) Background: The COVID-19 pandemic put a great burden on national healthcare systems, causing delays and disruptions in the medical care of non-COVID-19 patients. This paper aims to analyze the COVID-19 pandemic impact upon the quality of care in colorectal surgery. (2) Materials and Methods: We performed a retrospective study on the colorectal cancer cases operated in the Fourth Department of General Surgery, Emergency Hospital Bucharest Romania, over the period March 2020–February 2021 (pandemic group) vs. March 2019–February 2020 (non-pandemic group). (3) Results: The number of patients in the pandemic group decreased by 70% (36 vs. 118 patients), with lower accessibility from rural areas (11.1% vs. 37.2%, p = 0.035). Most cases in the pandemic group were emergencies (69% vs. 37.3%, p = 0.009), admitted for bowel obstruction (63.8% vs. 27.9%, p = 0.008). There was no in-hospital COVID-19 infection in patients operated for colorectal cancer. The 30-day mortality was significantly higher in the pandemic group (25% vs. 6.7%, p = 0.017), mostly due to septic shock (36.1% vs. 5%, p = 0.0001). (4) Conclusions: Colorectal cancer surgery may be performed safely during the COVID-19 pandemic, with strict adherence to the SARS-CoV-2 prevention protocols. However, the significant increase in colorectal cancers in the emergency was associated with worse outcomes and higher mortality during the COVID-19 pandemic.

1. Introduction

The COVID-19 pandemic has put enormous pressure on national health systems around the world for more than two years, both through a large number of hospitalizations, exceeding the capacity of intensive care beds and the frequent disruptions in health care for other conditions, conducting national screening programs during lockdown periods [1,2].
The standards of quality and safety were deeply affected by the rapid spread of the COVID-19 in all elements of Donabedian’s triad—structure, process, and outcomes, the global impact being difficult to quantify [3,4]. Hospitals encountered difficulties in balancing the resources of intensive care needed for COVID-19 patients while struggling to continue the routine hospital care. The prioritization of COVID-19 by health systems, non-COVID patients failed to receive appropriate care, missed scheduled check-ups for screening or procedures by imposed lockdowns, or were postponed by patients for fear of SARS-CoV-2 infection. Moreover, the staffing shortage, crush of work, and burnout among medical personnel had a direct impact on patient care, resulting in delayed or rushed care [5,6].
COVID-19 has reduced life expectancy in four-fifths of OECD countries [7]. Many studies raised concerns about the increased vulnerability of cancer patients during the COVID-19 pandemic, by limiting early access to diagnosis and treatment, discontinuation in treatment, and remission of controls due to travel restrictions and limited hospitalization [8,9,10]. A report on the COVID-19 pandemic impact on accessibility to chronic healthcare services in Romania showed a decrease by 35% in the oncological hospitalizations in 2020, in comparison with previous years [11]. Taking into account the gravity of oncological diseases and the importance of early diagnosis, there was a concern that this vulnerable segment could become a “silent collateral victim” of the COVID-19 pandemic [12,13,14]. After the first pandemic lockdown, national healthcare systems prioritized the access of oncological patients to adequate treatment facilities. However, in current practice, elective surgeries for digestive cancers were often delayed due to the lack of availability of intensive care beds. Colorectal cancer is the third most frequent malignancy worldwide, with an overall incidence of more than a million new cases per year [15], and one of the top causes of death by cancer [16].
This paper aims to analyze the challenges in surgical approaches to colorectal cancer encountered during the COVID-19 pandemic.

2. Materials and Methods

We conducted a retrospective comparative study on the patients diagnosed with colorectal cancer that underwent surgery in the Fourth Department of General Surgery, Emergency Hospital Bucharest, Romania, between March 2020 and February 2021 (pandemic group) vs. March 2019–February 2020 (non-pandemic group). March 2020 marked the beginning of the COVID-19 pandemic in our country. The data from the observation sheets and the operating protocols regarding emergency presentation, TNM staging, tumor location, therapeutic management, and changes in surgical practice protocols imposed by the COVID-19 pandemic were analyzed. The patients with colorectal cancer admitted for evaluation, for whom surgery was not performed, and patients admitted for bowel transit reconstruction after a temporary stoma were excluded. Quality of care was analyzed in terms of postoperative 30-day mortality and morbidity. Descriptive statistics were reported as percentages. The Student’s t-test was used to assess statistically significant correlations between continuous variables in the 2 study groups, and Wilcoxon (chi-squared) test for categorical variables. A p-value less than 0.05 was considered statistically significant. Data analysis was performed with the Statistical Software of SciStat® available at www.scistat.com (accessed on 15 January 2022) and IBM-SPSS22. Moreover, we also used the following statistical tests and models: Fisher’s exact test for contingency tables of dimension 2 × 2 (in order to compare frequencies) and dimension N × 2 for N > 2 (to compare discrete distributions); nonparametric Mann–Whitney U-test; binary multivariate logistic models and OR, the odds ratio statistic.

3. Results

3.1. Changes in Structure and Surgical Protocol during COVID-19 Pandemic

Before the COVID-19 pandemic, there were 54 hospital beds in our department. Between March 2019 and February 2020, 2404 patients were treated in our department, of which 1017 cases were admitted in emergency (42.3%), 1022 (42.5%) by planned admission and 365 (15.2%) were transferred from other departments. We identified 362 patients admitted with the ICD-10 code of colorectal cancer (codes C18-C20) between February 2019 and March 2020, out of which 118 were operated for the primary tumor and included in the present study.
During the first year of the COVID-19 pandemic (March 2020–February 2021), there were significant changes in the structure and circuits, to comply with the new regulations: social distancing for patients, with a minimum distance of 1.5 m between hospital beds and separate circuits for COVID-19 negative and COVID-19 suspects. The total number of beds decreased to 19 for COVID-19 negative patients and an additional area of 7 hospital beds for COVID-19 suspects, isolated one per room, until the result of the RT-PCR was obtained. A total of 1089 patients were hospitalized in the period March 2020–February 2021 in our department, out of which 514 (47.2%) in emergency, 313 (28.7%) by scheduled appointment and 262 (24%) were transferred from other departments. Our research identified 61 patients hospitalized with diagnostic codes C18-C20, out of which 36 were operated for colorectal cancer.
RT-PCR testing was routinely performed 24–48 h before the planned admission for elective surgery. Taking into account the early evidence of poor outcome in COVID-19 patients who underwent surgery [17,18], the admission was postponed in case of a positive result. For emergency presentations, RT-PCR was taken at admission, and the patient followed the circuits for COVID-19 suspects. If the patient’s condition permitted, surgery was delayed until the result of the RT-PCR was obtained. If the surgery had to be performed in emergency, all the precautions for a possible COVID-19 positive case were taken: full personal protective equipment (PPE), with N95 or FFP 2 or 3 (filtering facepiece) masks, eye protection, gowns, and gloves, limiting the maneuvers with risk of aerosolization, such as laparoscopy and limiting the exposure of healthcare personnel in the operating room to a minimum necessary, according to the current regulations for preventing SARS-CoV-2 infection [19,20]. Family visits were not permitted during the COVID-19 pandemic, except for special circumstances, such as imminent patient death.

3.2. General Data of the Patients Included in the Study Groups

The total number of colorectal cancer patients treated in our department between March 2020 and February 2021 was 70% lower when compared to the non-pandemic group (36 vs. 118 patients). Moreover, there was a significantly decreased addressability of patients from rural areas (11.1% vs. 37.2%, p = 0.035). This finding may be explained by several factors: the limitations in free circulation during lockdowns, the discontinuities in primary care, and patients’ decisions to postpone presentations due to fear of SARS-CoV-2 infection (Table 1).
There were no statistical differences in sex ratio between the 2 groups (p = 0.273). Age at presentation was slightly higher in the pandemic group (70.16+/−10.2 years vs. 66.6+/−11.2), but not statistically significant (p = 0.06). In both groups, the most frequent associated comorbidities were arterial hypertension, cardiac ischemic disease, and diabetes mellitus (Table 1). Preoperative chemotherapy was initiated at admission in 15.6% of cases in the non-pandemic group and only 5.5% of patients in the pandemic group. However, the statistical analysis did not find a significantly decreased value (p = 0.354).
Most patients in the pandemic group presented in emergency (69% vs. 37.3%, p = 0.009), with signs of bowel obstruction (63.8% vs. 27.9%, p = 0.008). The statistical analysis of the distribution of cases according to TNM stage revealed a higher incidence of loco-regional advanced colorectal tumors in the pandemic groups (T4 58.3% vs. 20.3%; N2 16.6% vs. 5.1%), but not statistically significant (p-value = 0.163).
An interesting finding in the histopathological exam was a significantly higher proportion of mucinous adenocarcinomas moderately differentiated (G2) in the pandemic group (72.2% vs. 17.6%. p = 0.002), while in the non-pandemic group, the most prevalent were conventional G2 colonic adenocarcinomas (59.3%). This type of colorectal tumor is generally associated with a delayed diagnosis until advanced stage, partial response to chemotherapy and worse outcomes compared with conventional colorectal adenocarcinoma [21,22].

3.3. Postoperative Outcomes in Pandemic and Non-Pandemic Groups

Tumor resection in intended oncological safety limits was performed in most cases in both groups (76.3% in the non-pandemic group, and 88.9% in the pandemic group, respectively). In the remaining cases, a colostomy or ileostomy was decided, either palliative or temporary, to resolve a bowel obstruction in emergency, in patients with multiple comorbidities and insufficiently explored as oncological status. Statistical analysis of the type of surgery showed no significant difference between the 2 study groups (Table 2).
The mean hospital stay was slightly lower in the pandemic group (12.72+/−5.3 days vs. 15.82+/−11.7 days). There was no in-hospital COVID-19 infection in patients operated for colorectal cancer, which proves the efficiency of the newly established circuits and procedures. The surgical wound infections were lower in the pandemic group, but not statistically significant. As a general guideline, colo-colic or colo-rectal anastomosis was avoided in cases operated in emergency, due to a high incidence of anastomotic leaks in such conditions. When analyzing the postoperative complications according to the Clavien Dindo classification (Table 3), the chi-square test did not show a significant difference among the 2 groups (p = 0.085). However, statistical analysis revealed worse outcomes in the pandemic group in terms of mortality (25% vs. 6.7%, p = 0.017) and postoperative septic shock (36.1% vs. 5%, p = 0.0001).
Furthermore, we assessed the differences in quality of care between the two study groups in terms of postoperative morbidity and in-hospital mortality. We found no significant differences in terms of hospital stay, wound related complications, Clostridium infection and acute cardiovascular complications, such as heart attack, malign arterial hypertension and acute pulmonary edema. However, we found an increased incidence of septic shock (p < 0.001) and death (p = 0.017) in the pandemic group.
A multivariate analysis was carried out in order to identify the main factors related to the worse outcome among the study groups (namely pandemic group and non-pandemic group). We investigated as covariates age, sex, emergency presentation, bowel occlusion, the associated diseases and major postoperative complications.
We used two logistic regression models: to compare pandemic/non- pandemic (Table 4); to compare death/non-death (Table 5).
The logistic regression model found for bowel occlusion an odds ratio OR (pandemic/non-pandemic) = exp(1.542) = 4.673 with 95% confidence interval CI = (1.905, 11.466) and for the septic shock, an odds ratio OR (pandemic/non-pandemic) = exp(2.87) = 17.932 with 95% confidence interval CI = (5.001, 64.301). The frequency of bowel occlusion and septic shock were significantly higher in pandemic period (the significance of goodness of fit test of Hosmer and Lemeshow Test is p = 0.592).
In a multivariate analysis of the factors that were associated with fatal outcome, we found that higher age (OR: 1.266, CI: 1.115–1.438), a higher number of comorbidities (OR: 2.681, CI: 1.189–6.049), the septic shock (OR: 15.828; CI: 2.944–85.094) and diabetes for the patients in the pandemic group (OR: 40.271; CI: 2.044–793.365) increased the death risk. For this model, the significance of Hosmer and Lemeshow Test is p = 0.606. Interestingly, for the patients in the non-pandemic group, diabetes was not associated with increased risk for fatal outcome. This may reflect an increased vulnerability of diabetic patients during the COVID-19 pandemic.
Septic shock was the most frequent cause of death in both groups, leading to a fatal outcome in 57.1% and 50% of cases with septic shock, respectively. However, the incidence of septic shock was significantly higher in patients admitted during COVID-19 pandemic, and this finding correlates significantly with emergency presentation.
Furthermore, we analyzed the possible correlations between emergency presentation and septic shock. We considered the questions, “Q1: Is emergency presentation a risk factor for septic shock?”, and, “Q2: To what extent did the COVID-19 pandemic influence the response to Q1?”. If all 154 cases are considered, statistical analysis shows that emergency presentation a risk factor for septic shock, with an estimate of odds ratio OR (Septic shock|Emergency presentation) = 5.155 and 95% confidence interval CI = (1.611, 16.488). However, this could be a misleading result for normal circumstances, with an OR of 1.714, but a wide 95% confidence interval CI = (0.233, 12.624).
When the statistical analysis was performed only on the pandemic group, the OR was considerably higher, of OR (septic shock|emergency presentation) = 4.154 with 95% confidence interval CI = (0.743, 23.229). The significance of this finding is yet of limited clinical value, due to the wide range of 95% CI, with subunitarian inferior limit. An explanation could be the small number of patients in pandemic-sample. On the other hand, multiple factors could impact the hospital care of patients admitted in emergency that experienced postoperative septic shock.

4. Discussion

The benchmarks of the quality of care in medical services are patient safety, effectiveness, timeliness, and patient-centered health service [23]. COVID-19 pandemic affected the quality of specialized healthcare services by multiple mechanisms. Kopel et al. found a significant decrease in diagnosis of colorectal cancers during the pandemic period, which could result in the long term in a devastating rise in late-stage CRC cases, and the overall loss of life years for these patients [24]. Health policy measures to save resources by reducing the overall number of surgeries during the COVID-19 pandemic also affect oncological colorectal resections [25]. While national health regulations promote a continuation of oncological surgical services, to prevent delays in diagnosis and treatment, the strained resources and manpower fatigue affect the quality of cancer care [26,27]. Discontinuities in screening, reduced referral, and accessibility to medical staff may result in delayed presentation, while discontinuity in regular check-ups may result in delayed diagnosis of recurrences [26]. Confronted with severe limitation of the resources and staff, several studies reported issues related to prioritization of cases, minimization of the risk of infection, and balancing the therapeutic options available [27,28]. Our hospital implemented major changes in structure and procedure, to safely treat both COVID-19-positive and COVID-19-negative patients during the entire pandemic period. The bed structure of the clinical departments was modified to create new available beds for COVID-19 patients, to the detriment of surgical departments. We were also confronted with reduced availability of intensive care beds, due to the increased number of COVID-19 patients requiring ventilatory support. All these changes led to a significant limitation of the number of complex surgeries during the COVID-19 pandemic, including colorectal cancers operations. On the other hand, the safety precautions and the new established circuits proved to be effective in SARS-CoV-2 infection prevention in the study group.
The surgical protocols in our department pay special attention to patient safety and the decrease in the postoperative complications, by routinely use of large spectrum antibiotics, perioperative anticoagulation for prevention of the thrombotic events, close perioperative care to prevent cardiac acute events, optimization of glycemia in diabetic patients, and prevention of postoperative pneumonia. However, operating complicated colorectal cancers in emergency remains challenging and it is associated with high postoperative mortality. While surgery for elective colorectal cancers is well standardized by national and local guidelines, the best option in cases of bowel obstruction in emergency is still a subject of debate. Min et al. found that all patients with obstruction due to colorectal cancer should undergo subtotal colectomy, based on the fact that staged operations are associated with higher mortality and morbidity and longer hospital stay in comparison to immediate resections [29]. However, adherence to traditional surgical oncologic principles and the goal to achieve R0 resection should be balanced with the patients’ biological status at presentation [30]. Clinical studies found 30-day postoperative mortality of 20% in patients with colorectal cancer operated in emergency in UK [15,31], and of 24% in Denmark [32] advising for damage-control surgery, such as colostomy, ileostomy, stenting or internal by-pass to solve obstruction. Patients with malignant colonic perforation face a high risk of peri-operative death, making septic source control the priority in the acute setting [31,33]. Age, Charlson comorbidity index, and tumor stage IV were associated with increased mortality of colorectal cancers operated in emergency [32].
The COVID-19 pandemic has brought important challenges in surgical practice, which we have never been confronted with before. In a systematic review of Mazidimoradi et al., the COVID-19 pandemic was found to have a negative effect both on the diagnosis and treatment of colorectal cancer [34]. Decreased diagnosis of new cases of colorectal cancer was seen in most countries, varying from 43.1% to 73.1% among different studies, with important discontinuities reported in screening programs and patients’ usual visits [34,35,36,37]. Clinical studies found a significant increase in emergency presentations, for bowel obstruction or perforation [33,34,35]. Suarez et al. found an increase in emergency presentation for colorectal cancer in Spain from 3.6% in 2019 to 12.1% in 2020 [38]. Shinkwin et al. found an increase in neoplastic bowel obstruction from 4.3% in 2019 to 8.6% in 2020, and draw attention that only a short delay of 4 months in referral and diagnosis leads to an increase in patients presenting with large bowel obstruction [39]. Our department is a tertiary center in the biggest emergency hospital in the country. This fact explains the increased proportion of complicated colorectal cases treated in emergency (37% before the COVID-19 pandemic and 72% during the first year of the COVID-19 pandemic), in comparison with other published studies.
In our research, we found significantly higher mortality in the pandemic group, which may be explained by the higher percentage of acute complicated cases. Emergency presentation of colorectal cancers has a severe impact upon patients’ survival and should be prevented. On the other hand, healthcare providers should balance the increased risk of death from COVID-19 exposure with preventable deaths from undertreating cancer patients [25,28,40]. Previously published reports found that elective colorectal surgical procedures may be safely performed during the pandemic, in the condition of establishing COVID-19 and non-COVID-19 circuits, strict visitor policy, and triage questionnaire for possible COVID-19 symptoms and RT-PCR testing before admission [24,27,41,42]. Our results verify previous reports, as we also registered no in-hospital SARS-CoV-2 infection in the pandemic group. This result may be a solid argument for encouraging colorectal elective surgery during COVID-19 pandemic, and preventing the future burden of advanced cases and the loss of life years for these patients.
The findings in the present research may support some recommendations to improve the outcomes of colorectal cancers patients admitted for surgery during the COVID-19 pandemic. In case of patients admitted in emergency for obstructive bowel cancer, minimal procedures, such as stenting or colostomy/ileostomy could be preferable to more extensive surgery, to decrease the risk of postoperative morbidity and mortality. Extensive lavage of peritoneal cavity, avoiding colonic anastomosis per primam, broad spectrum intravenous antibiotics and careful postoperative monitoring could be useful to prevent and treat septic shock.
Treating emergency colorectal patients is associated with worse outcomes, when compared to elective colorectal cancer surgery. In our country, oncological cases were treated continuously during pandemic waves, except the first lockdown period. However, in clinical practice, admission of elective oncological cases was often put on hold because of the lack of available ICU beds. Ensuring intensive care resources necessary for elective oncological surgery is mandatory for maintaining the standard of care in colorectal cancer surgery.
An increased mortality in the pandemic arm of the study has brought into question the use of strategies for bridging to elective surgery (BTS) such as self-expandable metal stents and decompression colostomies. Right sided colon malignancies are difficult to stent due to longer segments of poorly prepared bowel that need to be traversed compared to left sided obstructive lesions [43]. This is why we believe that in these cases, stoma is a more feasible alternative of BTS. Additionally, many authors advocate that inherent tumor manipulation during stenting could lead to local spreading or perforation rendering endoscopic procedures more dangerous and less compliant with the rigors of oncological principles [43,44,45,46]. However, one should consider that choosing decompression colostomies implies a three-stage procedure [47], while stenting offers a single stage surgery with primary anastomosis [45,46,48]. None of the patients in our study benefited of BTS because of the local policy and surgeon preferences, but we believe that the adoption of BTS should be considered in order to reduce mortality in emergency cases.
Our study has some limitations. The small number of patients included in the study may impact the statistical significance of the results. On the other hand, our hospital is an emergency hospital, and one may argue that chronic cancer patients were moreover treated in non-emergency hospitals. However, in our country, many of these hospitals were transformed in dedicated centers for COVID-19 patients only. Longer period and multicentric analysis could provide more comprehensive insight upon the effects of COVID-19 pandemic on the quality of care in colorectal oncological surgery. However, being a tertiary center, in the biggest emergency hospital in the country, our results raised awareness of the negative outcome of surgeries in emergency for colorectal cancer and postponing elective oncological surgeries.

5. Conclusions

The COVID-19 pandemic has deeply affected the quality of care in colorectal surgery, by decreasing the accessibility to healthcare surgical services, especially of people living in rural areas, and severe limitation of resources needed for perioperative intensive care. Colorectal cancer surgery may be performed safely during the COVID-19 pandemic, with strict adherence to the SARS-CoV-2 prevention protocols. However, the significant increase in colorectal cancers presentation in emergency is associated with worse outcomes and higher mortality during the COVID-19 pandemic and should be prevented.

Author Contributions

Conceptualization, D.S., G.V., C.T. (Corneliu Tudor), A.M.D. and C.G.S.; methodology, L.C.T., G.A.G. and C.G.S.; software, M.S.T., C.T. (Ciprian Tanasescu) and A.M.D.; validation, D.O.C., C.T. (Ciprian Tanasescu) and M.S.T.; formal analysis, S.A.B., D.D. and G.V.; investigation, D.S. and G.A.G.; resources, C.T. (Corneliu Tudor) and C.G.S.; data curation, G.V., D.D. and L.C.T.; writing—original draft preparation, D.S., S.A.B., A.M.D. and C.T. (Corneliu Tudor); writing—review and editing, G.V., G.A.G., D.O.C., D.D. and C.T. (Ciprian Tanasescu); visualization, G.A.G. and M.S.T.; supervision, D.S. and L.C.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Ethical review and approval were waived for this study due to the retrospective nature of the study.

Informed Consent Statement

Patient consent was waived due to the retrospective nature of the study.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. General data of the patients that underwent surgery for colorectal cancer in the 2 study groups (the percentages are calculated based on the total of the corresponding column, namely 118 and 36, respectively).
Table 1. General data of the patients that underwent surgery for colorectal cancer in the 2 study groups (the percentages are calculated based on the total of the corresponding column, namely 118 and 36, respectively).
ParameterNon-Pandemic Group
(March 2019–February 2020)		Pandemic Group
(March 2020–February 2021)		p Value
No. of cases11836
Females (no. of cases; %)36 (30.5%)16 (44.4%)0.158 (a)
Age (years)66.6+/−11.370.2+/−10.40.180 (b)
Rural vs. urban (no. of cases; %)44; 74 (37.2%; 72.8%)4; 32 (11.1%; 88.9%)0.003 * (a)
Emergency presentation (cases; %)44 (37.3%)25 (69%)0.009 * (a)
   • Occlusion33 (27.9%)23 (63.8%)0.008 * (a)
   • Perforation 2 (1.6%)1 (2.7%)0.367 (a)
   • Inferior digestive hemorrhage 9 (5%)1 (2.7%)0.685 (a)
Location of the tumor (no. of cases; %):
   • Cecum and right colon 30 (25.4%)10 (27.7%)0.829 (a)
   • Transverse colon 4 (3.3%)4 (11.1%)0.087 (a)
   • Left colon 51 (43.2%)17 (47.2%)0.704 (a)
   • Rectum/rectosigmoid 33 (27.9%)5 (13.8%)0.121 (a)
Chemotherapy before admission (no. of cases; %):16 (15.6%)2 (5.5%)0.354 (a)
Comorbidities (no. of cases; %):
   • Arterial hypertension 40 (33.9%)16 (44.4%)0.322
   • Ischemic coronary disease 30 (25.4%)20 (55.6%)0.001
   • Chronic respiratory diseases 18 (15.3%)0 (0.0%)0.008
   • Diabetes mellitus 10 (8.6%)4 (11.1%)0.741
   • Other 30 (25.4%)10 (27.8%)0.828
No. of comorbidities per patient: 0.273
   • ≥3 14 (11.8%)6 (16.6%)
   • 2 49 (41.5%)9 (25%)
   • 1 39 (33%)13 (36.1%)
   • 0 16 (13.5%)8 (22.2%)
TNM Stage (no. of cases; %)
T 0.163
    T212 (10.1%)0
    T367 (56.7%)12 (33.3%)
    T424 (20.3%)21 (58.3%)
    Tx9 (7.6%)3 (8.3%)
N 0.373
    N032 (27.1%)8 (22.2%)
    N172 (61%)18 (50%)
    N26 (5.1%)6 (16.6%)
    Nx8 (6.8%)4 (11.1%)
M 0.623
    M127 (22.8%)6 (16.6%)
    Mx91 (77.2%)30 (83.4%)
Histopathological forms (cases; %)
   • Colonic conventional adenocarcinoma 80 (67.68%)8 (22.1%)<0.001
   • Colonic mucinous adenocarcinoma 21 (17.8%)26 (72.2%)<0.001
   • Rectal adenocarcinoma NOS 11 (9.3%)00.196
   • Rectal squamous cell carcinoma 2 (1.6%)00.586
   • Neuroendocrine tumor 2 (1.6%)2 (5.5%)0.193
   • Colonic stromal tumor 2 (1.6%)00.586
Footnote: * Statistically significant (p < 0.05); (a) Fisher’s Exact Test for 2 × 2-Table; (b) Mann–Whitney U-test.
Table
Table 2. Types of surgery, mortality and postoperative complications in the 2 study groups.
Table 2. Types of surgery, mortality and postoperative complications in the 2 study groups.
Non-Pandemic GroupPandemic Groupp-Value
Type of surgery (no. of cases; %): 0.168 (c)
   • Rectum amputation 16 (13.5%)4 (11.1%)
   • Colostomy/ileostomy 29 (24.5%)5 (13.8%)
   • Hartman surgery 23 (19.4%)13 (36.1%)
   • Right hemicolectomy 27 (22.8%)8 (22.2%)
   • Left hemicolectomy 21 (17.7%)2 (5.5%)
   • Segmental resection 2 (1.7%)4 (11.1%)
Hospital stays (days)15.82+/−11.712.72+/−5.30.278 (b)
Postoperative hospital stays (days)11.59+/−9.411+/−4.940.798 (b)
Systemic postoperative complications (no. of cases; %):
   • Clostridium infection 12 (10.1%)5 (13.8%)0.452 (a)
   • Septic shock 6 (5%)13 (36.1%)<0.001 * (a)
   • Pulmonary acute edema 4 (3.3%)2 (5.5%)0.677 (a)
   • Myocardial infarction 2 (1.7%)0NS
   • Malign arterial hypertension 3 (2.5%)0NS
   • Urticaria 1 (0.9%)0NS
   • Urinary infection 2 (1.7%)0NS
Wound related complications (no. of cases; %):
   • Bleeding 3 (2.5%)0NS
   • SSI 16 (13.5%)4 (11.1%)NS
   • Infected hematoma 4 (3.3%)0NS
   • Anastomotic leak 8 (6.7%)4 (11.1%)NS
   • Colostomy detachment 1 (0.9%)0NS
Death at 30 days after surgery (no. of cases; %):8 (6.7%)9 (25%)0.017 * (a)
Causes of death (no. of cases; %):
   • Septic shock 4 (3.3%)8 (22.2%)<0.001 * (a)
   • Myocardial infarction 2 (1.7%)0NS
   • Pulmonary acute edema 2 (1.7%)1 (2.75%)NS
Footnote: * Statistically significant; NS: non-significant/irrelevant statistics; (a) Fisher’s Exact Test for 2 × 2-Table; (b) non-parametric Mann–Whitney U-test for comparison of distributions; (c) Fisher’s Exact Test for N × 2-Table, N > 2.
Table
Table 3. Postoperative morbidity in pandemic and non-pandemic groups according to the Clavien Dindo Classification of severity.
Table 3. Postoperative morbidity in pandemic and non-pandemic groups according to the Clavien Dindo Classification of severity.
Clavien Dindo Classification of Postoperative ComplicationsNon-Pandemic Group
(No. of Cases, %)		Pandemic Group
(No. of Cases, %)
Grade I (SSI, minor complications treated pharmacologically)17 (14.4%)2 (11.1%)
Grade II (treated pharmacologically)16 (13.5%)3 (16.6%)
Grade III13 (11%)4 (11.1%)
 IIIA (reintervention without general anesthesia)4 (3.3%)0
 IIIB (reintervention with general anesthesia)9 (7.6%)4 (11.1%)
Grade IV10 (8.4%)5 (13.8%)
 IVA (requiring ICU)4 (3.3%)2 (5.5%)
 IVB (with multiple organ failure)6 (5%)3 (8.3%)
Grade V8 (6.7%)9 (25%)
Table
Table 4. Logistic regression model for dependent variable pandemic/non-pandemic.
Table 4. Logistic regression model for dependent variable pandemic/non-pandemic.
IndependentBS.E.WalddfSig.OR (b) = Exp(B)95% C.I. for EXP(B)
VariableLowerUpper
Bowel occlusion01 (a)1.5420.45811.33410.0014.6731.90511.466
Septic shock01 (a)2.8870.65219.62810.00017.9325.00164.301
Constant−2.3270.35842.27810.0000.098
Footnote: (a) parameters with binary distribution; for logistic regression model calculation, it was used 0 = absent; 1 = present. (b) OR= odd ratio.
Table
Table 5. Logistic regression model for dependent variable death.
Table 5. Logistic regression model for dependent variable death.
IndependentBS.E.WalddfSig.OR(b) = Exp(B)95% C.I. for EXP(B)
VariableLowerUpper
age0.2360.06513.17410.0001.2661.1151.438
Number of comorbidities0.9860.4155.64810.0172.6811.1896.049
Septic shock 01 (a)2.7620.85810.35710.00115.8282.94485.094
Sample group × Diabetes01 (a)3.6961.5215.90510.01540.2712.044793.365
Constant−22.3895.49516.60310.0000.000
Footnote: (a) parameters with binary distribution; for logistic regression model calculation, it was used 0 = absent; 1 = present. Sample group = 1 for pandemic group and sample group = 0 for non-pandemic group; in the logistic regression model, diabetes resulted to be a risk factor for death only for the pandemic group; (b) OR= odd ratio.
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Serban, D.; Vancea, G.; Smarandache, C.G.; Balasescu, S.A.; Gangura, G.A.; Costea, D.O.; Tudosie, M.S.; Tudor, C.; Dumitrescu, D.; Dascalu, A.M.; et al. New Challenges in Surgical Approaches for Colorectal Cancer during the COVID-19 Pandemic. Appl. Sci. 2022, 12, 5337. https://doi.org/10.3390/app12115337

AMA Style

Serban D, Vancea G, Smarandache CG, Balasescu SA, Gangura GA, Costea DO, Tudosie MS, Tudor C, Dumitrescu D, Dascalu AM, et al. New Challenges in Surgical Approaches for Colorectal Cancer during the COVID-19 Pandemic. Applied Sciences. 2022; 12(11):5337. https://doi.org/10.3390/app12115337

Chicago/Turabian Style

Serban, Dragos, Geta Vancea, Catalin Gabriel Smarandache, Simona Andreea Balasescu, Gabriel Andrei Gangura, Daniel Ovidiu Costea, Mihail Silviu Tudosie, Corneliu Tudor, Dan Dumitrescu, Ana Maria Dascalu, and et al. 2022. "New Challenges in Surgical Approaches for Colorectal Cancer during the COVID-19 Pandemic" Applied Sciences 12, no. 11: 5337. https://doi.org/10.3390/app12115337

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