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Esophagectomy for Esophageal Cancer Performed During the Early Phase of the COVID-19 Pandemic

      Delay in time to esophagectomy for esophageal cancer has been shown to have worse peri-operative and long-term outcomes. We hypothesized that COVID-19 would cause a delay to surgery, with worse perioperative outcomes, compared to standard operations. All esophagectomies for esophageal cancer at a single institution from March-June 2020, COVID-19 group, and from 2019 were reviewed and peri-operative details were compared between groups. Ninety-six esophagectomies were performed in 2019 vs 37 during March-June 2020 (COVID-19 group). No differences between groups were found for preoperative comorbidities. Wait-time to surgery from final neoadjuvant treatment was similar, median 50 days in 2019 vs 53 days during COVID-19 p = 0.601. There was no increased upstaging, from clinical stage to pathologic stage, 9.4% in 2019 vs 7.5% in COVID-19 p = 0.841. Fewer overall complications occurred during COVID-19 vs 2019, 43.2% vs 64.6% p = 0.031, but complications were similar by specific grades. Readmission rates were not statistically different during COVID-19 than 2019, 16.2% vs 10.4% p = 0.38. No peri-operative mortalities or COVID-19 infections were seen in the COVID-19 group. Esophagectomy for esophageal cancer was not associated with worse outcomes during the COVID-19 pandemic with minimal risk of infection when careful COVID-19 guidelines are followed. Prioritization is recommended to ensure no delays to surgery.

      Graphical abstract

      Keywords

      Abbreviations:

      COVID-19 (Coronavirus Disease 2019)
      Unlabelled image
      Key Findings for Esophagectomies Performed During the Early COVID-19 Pandemic.
      Central Message
      Esophagectomy for esophageal cancer can safely be performed during the COVID-19 pandemic.
      Perspective Statement
      Delays in esophagectomy for esophageal cancer lead to worsened long-term outcomes. With the ongoing challenges of the COVID-19 pandemic we demonstrate that, with appropriate precautions, esophagectomies can proceed with similar short-term outcomes and minimal risk of COVID-19 infection. Prioritization of surgical care for these patients is recommended.

      INTRODUCTION

      Coronavirus-19 has significantly affected healthcare globally. The safety of surgery and postoperative care for esophageal cancer patients who undergo esophagectomy during the pandemic is of particular concern due to the virus's multisystem effects that may impact the operation.
      • Zaim S
      • Chong JH
      • Sankaranarayanan V
      • et al.
      COVID-19 and multiorgan response.
      ,
      • Lazzaroni MG
      • Piantoni S
      • Masneri S
      • et al.
      Coagulation dysfunction in COVID-19: The interplay between inflammation, viral infection and the coagulation system.
      During the coronavirus pandemic the screening, administration of chemotherapy, and surgical management of multiple cancers has been shown to be heavily impacted.
      • Patt D
      • Gordan L
      • Diaz M
      • et al.
      Impact of COVID-19 on cancer care: how the pandemic is delaying cancer diagnosis and treatment for american seniors.
      Due to the aggressive nature of esophageal cancer, delays in treatment are not advised and esophageal cancer patients have priority when resources are available.
      • M Antonoff
      • Backhus L
      • et al.
      Thoracic Surgery Outcomes Research Network, Inc
      COVID-19 guidance for triage of operations for thoracic malignancies: A consensus statement from Thoracic Surgery Outcomes Research Network.
      However, patients who undergo neoadjuvant chemoradiation therapy typically require a brief recovery period before proceeding to definitive surgery. The ideal duration between neoadjuvant therapy and surgery remains under debate both in terms of peri-operative outcomes and long-term survival and is of paramount importance during the ongoing pandemic.
      • Kim JY
      • Correa AM
      • Vaporciyan AA
      • et al.
      Does the timing of esophagectomy after chemoradiation affect outcome?.
      ,
      • Qin Q
      • Xu H
      • Liu J
      • et al.
      Does timing of esophagectomy following neoadjuvant chemoradiation affect outcomes? A meta-analysis.
      We hypothesized that esophagectomies performed during the COVID-19 pandemic would be delayed with more complications and worse peri-operative complications and mortality compared to one year before the pandemic.

      METHODS

      The Institutional Review Board (IRB) or equivalent ethics committee of the Brigham and Women's Hospital approved the study protocol and publication of data. Patient written consent for the publication of the study data was waived by the IRB due to the retrospective nature of the study. Retrospective review of the charts of all patients who underwent esophagectomy for esophageal cancer at our institution from January 1, 2019, to December 31, 2019 (pre-COVID-19 group) and March 1, 2020 to June 30, 2020 (COVID-19 group) was performed. After June 30, 2020, the monthly rate of esophagectomies returned to pre-pandemic levels and differences were no longer expected to be observed. Esophagectomies performed for benign conditions were excluded. Demographic and comorbidity variables included were age, gender, body mass index (BMI), Barrett's esophagus, pre-operative atrial fibrillation, history of other cancer, congestive heart failure, coronary artery disease, chronic obstructive pulmonary disease, hypertension, diabetes, and smoking history. Clinical stage by endoscopic ultrasound, neoadjuvant treatment status, and time to surgery from either last neoadjuvant treatment or clinic visit (in the case of patients who did not undergo neoadjuvant therapy) were also collected. All operations were performed via a McKeown or Ivor Lewis technique. Surgical approach was categorized as open, minimally invasive (thoracoscopy or laparoscopy), or robotic based on the final technique when the operation was concluded. Overall approach was classified as open if both the thoracic and abdominal portions were via open technique, minimally invasive if both the thoracic and abdominal portions were via minimally invasive or robotic technique, or hybrid if there was a combination of minimally invasive and open techniques. Pathologic variables included histology, margins, lymph node details, microscopic invasion details, pathologic stage, and change of clinical stage to pathologic stage. Outcomes examined were initial intensive care unit length of stay, overall complications and complications by Clavien-Dindo grade, intensive care unit readmission, any additional procedures performed postoperatively, and mortality out to 90 days after surgery. Complications were graded on the Clavien-Dindo system of surgical complications; Grade III and higher was considered significant.
      • Dindo D
      • Demartines N
      • Clavien PA.
      Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey.
      Time to first follow-up was collected for the COVID-19 group.

      Analysis

      Values were compared between groups using Chi-square test, Wilcoxon rank-sum test, and Fisher's exact test, where appropriate. A p value equal to or less than 0.05 was considered significant. All statistical tests were performed with STATA version 14 (StataCorp. 2015. Stata Statistical Software: Release 14. College Station, TX: StataCorp LP)

      Institutional Changes to Respond to Coronavirus-19 infection

      As part of our institutional pandemic response, all surgical patients were required to have a negative COVID-19 test within 72 hours before surgery and were directed to self-quarantine from the time of their COVID test until day of surgery. Hospital staff completed daily symptom attestations before work and were required to wear masks while in the hospital. Visitors were restricted to one two-hour visit with a single visitor between 1-8PM daily. No visitors were allowed in the ICU. Esophagectomy patients were in the same ICU as COVID-19 patients at the start of the study prior to creation of COVID-19 ICUs. Every patient was tested every 3 days for COVID-19 during their inpatient stay and each patient had a private room.

      RESULTS

      Thirty-seven esophagectomies were performed between March and June at our institution vs 96 in 2019. Four cases were done during mid-March to mid-April 2020 when the operating rooms were reserved only for emergency cases and the institution had the largest number of COVID-19 patients in the hospital. These cases were performed only after careful discussion with the patient, referring doctors, and operating room administrators. During this study, no patient was diagnosed with, or had COVID-19 symptoms during their hospitalization or by first follow-up.
      Age, gender, BMI, Barrett's esophagus, hypertension, pre-operative atrial fibrillation, history of other cancer, congestive heart failure, coronary artery disease, chronic obstructive pulmonary disease, diabetes, and smoking history were similar between groups, Table 1. Clinical stages were similar between groups. Both groups had similar rates of neoadjuvant chemoradiation (89.6% in 2019 vs 94.6% during COVID-19, p = 0.509). Median time to surgery from last neoadjuvant treatment was similar between groups (50 days in 2019 vs 53 days during COVID-19 p = 0.601).
      Table 1Esophagectomy for Esophageal Cancer during COVID-19 Pandemic Compared to 2019: Pre-operative Demographics, Comorbidities, Clinical Staging, Neoadjuvant Treatment, and Time to Surgery
      2019 GroupCOVID-19 Groupp-value
      VariableNumber of patients (n total = 96)%Number of patients (n total = 37)%
      Age, yearsMedian (IQR)66.3560.3, 71.766.3459.4, 72.90.952
      Gender, Male7881.253286.490.612
      Body Mass Index (BMI)Median (IQR)28.024.4, 32.328.024.8, 32.30.914
      Barrett's esophagus2728.135.0013.510.112
      Pre-operative Atrial Fibrillation1414.583.008.110.396
      History of Other Cancer1818.7510.0027.030.344
      Congestive Heart Failure44.170.000.000.576
      Coronary Artery Disease1313.544.0010.810.779
      Chronic Obstructive Pulmonary Disease1212.505.0013.511.00
      Hypertension6264.5817.0045.950.075
      Diabetes1515.638.0021.620.447
      SmokerNever2121.888.0021.620.678
      Current1919.7910.0027.03
      Former5658.3319.0051.35
      Clinical StageStage I6.06.33.08.10.708
      (EUS)Stage II10.010.43.08.11.000
      Stage III40.041.723.062.20.052
      Stage IVa9.09.42.05.40.727
      Stage IVb2.02.11.02.71.000
      Not Reported29.030.25.013.50.074
      Neoadjuvant Chemoradiation Therapy8689.583594.590.509
      Chemotherapy Only11.0400
      Radiation Therapy Only0000
      Surgery Only99.3825.41
      Time to Surgery, daysMedian (IQR)5040, 675337.5, 63.50.601
      from Last Dose of Neoadjuvant Treatment
      COVID-19, coronavirus disease 2019; COVID-19 group, esophagectomy patients from March-June 2020; 2019 group, esophagectomy patients from calendar year 2019; IQR, interquartile range for non-normal distribution data with 25th and 75th percentiles; BMI, body mass index in kg/m2; EUS, endoscopic ultrasound.
      All cases were done via McKeown or Ivor Lewis technique in both groups with approximately 70% being performed with Ivor Lewis technique, Table 2. There were trends of more minimally invasive operations during 2019 (83.3% vs 73.0%, p = 0.223) and more COVID-19 group operations completed via a hybrid surgical approach (21.6% patients during COVID-19 vs 8.3% in 2019, p = 0.070). More cases had a robotic abdominal approach in 2019 (19.8% vs 2.7% p=0.013) but conversion rates were similar between groups, Table 2. Median tumor size was larger during COVID-19 (4.2 cm vs 3.0 cm in 2019, p < 0.01). Rates of downstaging, from clinical stage to pathologic staging, and upstaging were no different between groups with approximately 60% of patients in both groups being down staged from their pre-operative clinical stage. Initial ICU stay was a median of 2 days in both groups but with more long duration stays in 2019, Table 3. Median length of stay was shorter during COVID-19 (7 vs 9 days in 2019, p < 0.01). Overall complications and Grade IV, and V complications were no different between groups. Grade III complications were trended towards being more common in 2019 but did not reach significance (33.3% vs 16.2% COVID-19, p = 0.056). Anastomotic leak rate was 10.8% during COVID-19 vs 6.3% during 2019, p = 0.464. Additional postop procedure rate, 30-day mortality and 90-day mortality were similar between groups. Readmission rate was 16.2% during COVID-19 vs 10.4% in 2019, p = 0.38.
      Table 2Esophagectomy for Esophageal Cancer during COVID-19 Pandemic Compared to 2019: Operative Details, Final Pathology and Staging
      2019 GroupCOVID-19 Groupp-value
      VariableNumber of patients (n total = 96)%Number of patients (n total = 37)%
      Surgical TechniqueMcKeown29.030.210.027.00.833
      Ivor Lewis67.069.827.073.0
      Approach - OverallMIE80.083.327.073.00.223
      Open8.08.32.05.40.726
      Hybrid- open and MIE8.08.38.021.60.070
      Approach - ThoracicMIE64.066.721.056.80.318
      Open12.012.54.010.81.000
      Robotic20.020.812.032.40.179
      Approach - AbdominalMIE65.067.728.075.70.407
      Open12.012.58.021.60.189
      Robotic19.019.81.02.70.013
      Convert-to-openThoracic3.03.11.02.70.842
      Abdominal1.01.01.02.7
      Both1.01.00.00.0
      Tumor Size, cmMedian (IQR)31.8, 3.64.23.3, 5.5<0.01
      HistologyAdenocarcinoma7477.083183.780.11
      Squamous Cell Carcinoma1212.5616.22
      Other1010.4200
      Lymph nodes, SampledMedian (IQR)2116, 272517, 300.265
      Lymph nodes, PositiveMedian (IQR)00, 1.300, 20.64
      Lymphovascular Invasion Present1818.751129.730.24
      Perineural Invasion Present1212.50924.320.113
      Pathologic Stage at SurgeryStage I5153.131643.240.336
      Stage II1212.50616.22
      Stage III88.3338.11
      Stage IVa2222.92821.62
      Stage IVb22.08410.81
      Stage IVb M111.0400.00
      n = 67%n = 32%
      Overall Change in StageDownstage4364.1819.0059.380.841
      (Clinical Stage to Final Pathologic stage)Upstage57.463.009.38
      Same stage1928.3610.0031.25
      COVID-19, coronavirus disease 2019; COVID-19 group, esophagectomy patients from March-June 2020; 2019 group, esophagectomy patients from calendar year 2019; IQR, interquartile range for non-normal distribution data with 25th and 75th percentiles; MIE, minimally invasive esophagectomy
      Table 3Esophagectomy for Esophageal Cancer during COVID-19 Pandemic Compared to 2019: Peri-operative Morbidity and Mortality
      2019 GroupCOVID-19 Groupp-value
      VariableNumber of patients (n total = 96)%Number of patients (n total = 37)%
      Initial Intensive Care Unit Length of StayMedian (IQR)2.01, 32.01, 20.019
      Length of Stay, daysMedian (IQR)98, 1277, 10<0.01
      Post-operative Complications3334.38718.920.094
      Grade III3233.33616.220.056
      Grade IV99.38513.510.533
      Grade V22.0812.701
      Anastomotic Leak6.06.34.010.80.464
      Intensive Care Unit Readmission8.08.33.08.11.000
      Additional Post-operative Procedure25.026.010.027.01.000
      Major Reoperation12.012.55.013.51.000
      Minor Reoperation13.013.55.013.51.000
      Readmitted within 30 days10.010.46.016.20.38
      30-day Mortality22.08001
      90-day mortality44.2025.400.670
      Note: Complications were graded according to the Clavien-Dindo complication grading system. Minor reoperations consisted of tracheostomies, upper endoscopies, or bedside incision and drainage procedures. Major operations were those performed under general anesthesia to address significant complications.
      COVID-19, coronavirus disease 2019; COVID-19 group, esophagectomy patients from March-June 2020; 2019 group, esophagectomy patients from calendar year 2019; IQR, interquartile range for non-normal distribution data with 25th and 75th percentiles
      A summary of the key findings and their implications can be found in Figure 1.
      Figure 1
      Figure 1Graphical Abstract of Esophagectomy for Esophageal Cancer Safely Performed During COVID-19 Pandemic showing summary of methods, results, and implications.

      DISCUSSION

      Esophagectomy for esophageal cancer was not associated with worse outcomes during the COVID-19 pandemic with minimal risk of infection when careful COVID-19 guidelines were followed. Our institution underwent an operating room shutdown in mid-March 2020 to mid-April 2020. Only emergencies and carefully considered cases were performed. As semi-elective operations were resumed there was a backlog of patients who were at risk significantly delayed surgery. Esophageal cancer cases were prioritized in the initial phase when the operating rooms were reopened due to their high-risk nature and to attempt to minimize the length of time from the completion of neoadjuvant therapy to surgery, if applicable. We found these efforts were successful.
      With institutional protocols put in place before guidelines were more common, none of our patients were infected with COVID-19 during their post-operative admission or by their first follow-up appointment. This allowed us to avoid many of the pulmonary complications and mortality that had been reported elsewhere.
      COVIDSurg Collaborative
      Mortality and pulmonary complications in patients undergoing surgery with perioperative SARS-CoV-2 infection: an international cohort study.
      Our institution did not set up full COVID-19-free surgical pathways (dedicated operating room, critical care, and inpatient wards) as noted in Glasbey et al. but dedicated critical care and inpatient wards were set up later in our study period.
      • Glasbey JC
      • Nepogodiev D
      • Simoes JFF
      • et al.
      Elective cancer surgery in COVID-19-free surgical pathways during the SARS-CoV-2 pandemic: an international, multicenter, comparative cohort study.
      In the early portion of the pandemic there was debate regarding the possible aerosolization of the virus during laparoscopy.
      • Angioni S.
      Laparoscopy in the coronavirus disease 2019 (COVID-19) era.
      • Mintz Y
      • Arezzo A
      • Boni L
      • et al.
      The risk of COVID-19 transmission by laparoscopic smoke may be lower than for laparotomy: a narrative review.
      • Wang J
      • Du G.
      COVID-19 may transmit through aerosol.
      Larger tumor sizes were also seen during the pandemic, but conversion rate was similar to 2019. We do not believe these factors impacted our rate of open abdominal surgery as one surgeon customarily uses laparotomy for the abdominal portion of esophagectomies and the conversion rate was no different.
      The increased, statistically nonsignificant, rate of anastomotic leaks seen during COVID-19 were not related to the pandemic and are within the range of recent studies.
      • Kaufman HW
      • Chen Z
      • Niles J
      • et al.
      Changes in the number of US patients with newly identified cancer before and during the coronavirus disease 2019 (COVID-19) pandemic.
      • Manghelli JL
      • Ceppa DP
      • Greenberg JW
      • et al.
      Management of anastomotic leaks following esophagectomy: when to intervene?.
      • Chidi AP
      • Etchill EW
      • Ha JS
      • et al.
      Effect of thoracic versus cervical anastomosis on anastomotic leak among patients who undergo esophagectomy after neoadjuvant chemoradiation.
      Upon inspection of our morbidity database from March 2020 through February 2021, 9 leaks occurred during the year with 4 during our study period for COVID-19. The annualized rate for leaks is 9.5% (9/95) compared to 5.2% (5/96) in 2019. For the COVID-19 cases, one case had technical intraoperative issues, 2 of the leaks were noted on upper gastrointestinal series done per standard post-operative esophagectomy protocols, and the final 2 patients had leaks noted 9 and 11 days after surgery which required additional procedural management. The causes for this increase in leak rate since COVID-19 started are currently under investigation.
      Lastly, length of stay was shorter during the pandemic in part due to concerns for patients staying longer in the hospital but was accompanied by a higher readmission rate. The total readmission rate from March 2020 through February 2021 is 12.6% (12/95). Upon further review of the causes for readmission, none of the patients were readmitted for COVID-19 related issues. Examples include, delayed esophageal leak, failure to thrive, and dysphagia.
      The lessons we learned in this early experience dealing with a respiratory pandemic were myriad. Due to the progressive nature of esophageal cancer, significant efforts to ensure timely scheduling of operations after completion of neoadjuvant treatment is necessary. Next, staying current on the developing literature, guidelines, and reports of disease transmission to update pre-admission, and during hospitalization, COVID-19 testing strategies should be done. Additionally, hospital staff adherence to strict mask and symptom reporting policies to prevent potential iatrogenic COVID-19 transmission are mandatory. Clear discussions with patients on how to prevent getting COVID-19 before admission as well as restricting visitors is essential to further reduce transmission risk. Once patients are in the hospital, every effort to perform esophagectomies by minimally invasive methods and keep the conversion rate to a minimum help maintain transmission safety and reduce complications of esophagectomy. Since strict visitor restrictions are necessary to prevent infection from non-patient and non-hospital staff sources, the hospital should provide increased social support services and technology for patients to communicate with outside family and friends. After discharge, close 2-week follow-up by either in-person visit or tele-medicine is key to help monitor patients postoperatively, remind them of best practices for preventing COVID-19 infection, and attempt to reduce readmission. Later in the pandemic, our successful and safe results of the first few brave patients were able to be communicated to subsequent patients. This helped reassure them that coming to the hospital for their surgery was safe.
      Some limitations and possible biases may have been introduced. During resumption of semi-elective cases, patient selection bias may have occurred that may have not been captured in our data leading to decreased complication rates during COVID-19. The emphasis placed on rapid discharge to minimize COVID-19 exposure may have contributed to the higher, non-significant, readmission that was observed in the COVID-19 group. An additional limitation is the low number of patients operated on during he pandemic.
      We expect no difference in long-term outcomes for the COVID-19 group compared to previous patients since there was no increased rate of complications or upstaging on pathology. Continued observation is warranted as the pandemic progresses to ensure esophageal cancer patients who need to be evaluated and treated receive appropriate care.
      • Kamarajah SK
      • Lin A
      • Tharmaraja T
      • et al.
      Risk factors and outcomes associated with anastomotic leaks following esophagectomy: a systematic review and meta-analysis.

      CONCLUSIONS

      During the ongoing COVID-19 pandemic, with appropriate case prioritization, preoperative testing, staff policies, and systemwide measures, esophagectomy for esophageal cancer was not associated with worse perioperative outcomes and minimal risk of infection with COVID-19 at our institution.

      Supplementary Material

      REFERENCES

        • Zaim S
        • Chong JH
        • Sankaranarayanan V
        • et al.
        COVID-19 and multiorgan response.
        Curr Probl Cardiol. 2020; 45100618https://doi.org/10.1016/j.cpcardiol.2020.100618
        • Lazzaroni MG
        • Piantoni S
        • Masneri S
        • et al.
        Coagulation dysfunction in COVID-19: The interplay between inflammation, viral infection and the coagulation system.
        Blood Rev. 2020; ([published online ahead of print, 2020 Aug 24])100745https://doi.org/10.1016/j.blre.2020.100745
        • Patt D
        • Gordan L
        • Diaz M
        • et al.
        Impact of COVID-19 on cancer care: how the pandemic is delaying cancer diagnosis and treatment for american seniors.
        JCO Clin Cancer Inform. 2020; 4 (PMID: 33253013 PMCID: PMC7713534): 1059-1071https://doi.org/10.1200/CCI.20.00134
        • M Antonoff
        • Backhus L
        • et al.
        • Thoracic Surgery Outcomes Research Network, Inc
        COVID-19 guidance for triage of operations for thoracic malignancies: A consensus statement from Thoracic Surgery Outcomes Research Network.
        J Thorac Cardiovasc Surg. 2020; 160 (Epub 2020 Apr 9. PMID:32689703PMCID: PMC7146695): 601-605https://doi.org/10.1016/j.jtcvs.2020.03.061
        • Kim JY
        • Correa AM
        • Vaporciyan AA
        • et al.
        Does the timing of esophagectomy after chemoradiation affect outcome?.
        Ann Thorac Surg. 2012; 93 (discussion 212-3. Epub 2011 Oct 1PMID:21962263PMCID: PMC4041623): 207-212https://doi.org/10.1016/j.athoracsur.2011.05.021
        • Qin Q
        • Xu H
        • Liu J
        • et al.
        Does timing of esophagectomy following neoadjuvant chemoradiation affect outcomes? A meta-analysis.
        Int J Surg. 2018; 59 (Epub 2018 Sep 24. PMID:30261331): 11-18https://doi.org/10.1016/j.ijsu.2018.09.013
        • Dindo D
        • Demartines N
        • Clavien PA.
        Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey.
        Ann Surg. 2004; 240 (PMID:15273542 PMCID: PMC1360123): 205-213https://doi.org/10.1097/01.sla.0000133083.54934.ae
        • COVIDSurg Collaborative
        Mortality and pulmonary complications in patients undergoing surgery with perioperative SARS-CoV-2 infection: an international cohort study.
        Lancet. 2020; 396 (Epub 2020 May 29. Erratum in: Lancet. 2020 Jun 9;: PMID:32479829 PMCID: PMC7259900): 27-38https://doi.org/10.1016/S0140-6736(20)31182-X
        • Glasbey JC
        • Nepogodiev D
        • Simoes JFF
        • et al.
        Elective cancer surgery in COVID-19-free surgical pathways during the SARS-CoV-2 pandemic: an international, multicenter, comparative cohort study.
        J Clin Oncol. 2021; 39 (Epub 2020 Oct 6. PMID:33021869): 66-78https://doi.org/10.1200/JCO.20.01933
        • Angioni S.
        Laparoscopy in the coronavirus disease 2019 (COVID-19) era.
        Gynecol Surg. 2020; 17 (Epub 2020 May 14. PMID:32435173PMCID: PMC7224160): 3https://doi.org/10.1186/s10397-020-01070-7
        • Mintz Y
        • Arezzo A
        • Boni L
        • et al.
        The risk of COVID-19 transmission by laparoscopic smoke may be lower than for laparotomy: a narrative review.
        Surg Endosc. 2020; 34: 3298-3305https://doi.org/10.1007/s00464-020-07652-y
        • Wang J
        • Du G.
        COVID-19 may transmit through aerosol.
        Ir J Med Sci. 2020; 189: 1143-1144https://doi.org/10.1007/s11845-020-02218-2
        • Kaufman HW
        • Chen Z
        • Niles J
        • et al.
        Changes in the number of US patients with newly identified cancer before and during the coronavirus disease 2019 (COVID-19) pandemic.
        JAMA Netw Open. 2020; 3e2017267https://doi.org/10.1001/jamanetworkopen.2020.17267
        • Manghelli JL
        • Ceppa DP
        • Greenberg JW
        • et al.
        Management of anastomotic leaks following esophagectomy: when to intervene?.
        J Thorac Dis. 2019; 11: 131-137https://doi.org/10.21037/jtd.2018.12.13
        • Chidi AP
        • Etchill EW
        • Ha JS
        • et al.
        Effect of thoracic versus cervical anastomosis on anastomotic leak among patients who undergo esophagectomy after neoadjuvant chemoradiation.
        J Thorac Cardiovasc Surg. 2020; 160 (Epub 2020 Feb 20. PMID:32299695): 1088-1095https://doi.org/10.1016/j.jtcvs.2020.01.089
        • Kamarajah SK
        • Lin A
        • Tharmaraja T
        • et al.
        Risk factors and outcomes associated with anastomotic leaks following esophagectomy: a systematic review and meta-analysis.
        Dis Esophagus. 2020; 33 (PMID:31957798): doz089https://doi.org/10.1093/dote/doz089

      Linked Article

      • Commentary: Cancer Cannot Wait – Esophagectomy During the COVID-19 Pandemic
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          During the height of the pandemic, elective healthcare was cancelled to preserve hospital resources for the influx of patients suffering from COVID-19. Many centers continued to offer cancer care; however, resource limitations affected care in ways that have yet to be fully described. Healthcare teams were “learning on the go” to design processes that would allow for continued treatment of cancer, while battling a contagious virus that threatened patients and providers alike. It was unknown at the time if laparoscopy would endanger the esophagectomy team present in the operating room.
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      • Commentary: SARS-CoV-2 and Esophagectomy for Esophageal Cancer: Timely Operations and Good Outcomes
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          The novel coronavirus SARS-CoV-2, commonly known as COVID-19, presented a challenge for all medical professionals. Many hospitals and health systems were overwhelmed with sick infected patients. Lack of protective equipment and fully occupied emergency rooms and intensive care units caused a delay in treating other conditions, often with deleterious effects on patients' health. Another important issue during the pandemic was the unknown consequence of COVID-19 infection in the perioperative period.
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