Prevention of COVID-19 in Thoracic Surgery Patients: Lessons Learned during the First Pandemic Wave

Abstract

Background The aim of this retrospective study was to investigate the implementation of measures to prevent perioperative COVID-19 in thoracic surgery during the first wave of the COVID-19 pandemic 2020 allowing a continued surgical treatment of patients.

Methods The implemented preventive measures in patient management of the thoracic surgery department of the Asklepios Lung Clinic Munich-Gauting, Germany were retrospectively analyzed. Postoperative COVID-19 incidence before and after implementation of preventive measures was investigated. Patients admitted for thoracic surgical procedures between March and May 2020 were included in the study. Patient characteristics were analyzed. For the early detection of putative postoperative COVID-19 symptoms, typical post-discharge symptomatology of thoracic surgery patients was compared to non-surgical patients hospitalized for COVID-19.

Results Thirty-five surgical procedures and fifty-seven surgical procedures were performed before and after implementation of the preventive measures, respectively. Three patients undergoing thoracic surgery before implementation of preventive measures developed a COVID-19 pneumonia post-discharge. After implementation of preventive measures, no postoperative COVID-19 cases were identified. Fever, dyspnea, dry cough and diarrhea were significantly more prevalent in COVID-19 patients compared to normally recovering thoracic surgery patients, while anosmia, phlegm, low energy levels, body ache and nausea were similarly frequent in both groups.

Conclusions Based on the lessons learned during the first pandemic wave, we here provide a blueprint for successful easily implementable preventive measures minimizing SARS-CoV-2 transmission to thoracic surgery patients perioperatively. While symptoms of COVID-19 and the normal postoperative course of thoracic surgery patients substantially overlap, we found dyspnea, fever, cough, and diarrhea significantly more prevalent in COVID-19 patients than in normally recovering thoracic surgery patients. These symptoms should trigger further diagnostic testing for postoperative COVID-19 in thoracic surgery patients.

Zusammenfassung

Hintergrund Ziel dieser retrospektiven Studie war die Untersuchung von Maßnahmen zur Prävention perioperativer COVID-19-Erkrankungen bei fortgesetztem Vollbetrieb der Thoraxchirurgie während der ersten Welle der COVID-19-Pandemie 2020.

Methoden Es erfolgte eine retrospektive Analyse von eingesetzten Präventionsmaßnahmen in der Abteilung für Thoraxchirurgie der Asklepios Lungenklinik München-Gauting. Hierzu wurde die Inzidenz postoperativer COVID-19-Erkrankungen vor und nach der Einführung der Präventionsmaßnahmen ausgewertet. Patienten mit thoraxchirurgischen Operationen zwischen März und Mai 2020 wurden in die Studie eingeschlossen. Durch den Vergleich der postoperativen Symptome thoraxchirurgischer Patienten mit Symptomen von COVID-19-Patienten wurden spezifische Symptome zur Früherkennung der postoperativen COVID-19-Erkrankung identifiziert.

Ergebnisse Vor Einführung der Präventionsmaßnahmen erfolgten 35 thoraxchirurgische Operationen innerhalb von 22 Tagen während hoher COVID-19-Prävalenz im Einzugsgebiet der Klinik. Nach Einführung der Präventionsmaßnahmen erfolgten 57 thoraxchirurgische Eingriffe innerhalb von 54 Tagen. Vor Umsetzung der Präventionsmaßnahmen entwickelten 3 Patienten postoperativ eine COVID-19-Pneumonie. Nach Umsetzung zeigte sich kein postoperativer COVID-19-Fall. Fieber, Atemnot, trockener Husten und Durchfall waren bei an COVID-19 erkrankten Patienten signifikant häufiger als bei thoraxchirurgischen Patienten mit regelhaftem postoperativem Verlauf. Anosmie, Auswurf, Abgeschlagenheit, Gliederschmerzen und Übelkeit traten in beiden Gruppen ähnlich häufig auf.

Schlussfolgerungen Basierend auf unseren Erfahrungen in der ersten Pandemiewelle bieten wir eine Blaupause für erfolgreiche, leicht umzusetzende präventive Maßnahmen zur Minimierung des Risikos für eine perioperative COVID-19-Erkrankung bei thoraxchirurgischen Patienten. Wir konnten zeigen, dass Symptome einer postoperativen COVID-19-Pneumonie teilweise schwer von klassischen postoperativen Beschwerden abgrenzbar sind. Postoperative Dyspnoe, Fieber, Husten und Diarrhöen traten jedoch signifikant häufiger bei COVID-19-Erkrankten als im postoperativen Verlauf thoraxchirurgischer Patienten auf und sollten daher differenzialdiagnostisch an eine postoperative COVID-19-Erkrankung denken lassen.

Abbreviations

BMI: Body Mass Index

COVID-19: Coronavirus disease 2019

CT: Computer tomography

IQR: Interquartile range

LMU: Ludwig-Maximilians-University

PCR: Polymerase chain reaction

SARS-CoV-2: Severe acute respiratory syndrome coronavirus 2

Introduction

COVID-19 is an infectious disease caused by the SARS-CoV-2 virus, first described in December 2019 that became pandemic in the first quartile of 2020 [1] [2]. The rapid pandemic spread of SARS-CoV-2 virus and the consecutive alarming COVID-19-related morbidity and mortality enforced emergent changes in patient management across all medical and surgical specialties and sub-specialties including thoracic surgery [1] [2].

As previously reported by our [3] and other groups [4], postoperative COVID-19 represents a severe threat to the postoperative patient health. Therefore, continued treatment of patients in need of thoracic surgery requires an effective screening of patients for symptomatic and asymptomatic COVID-19 prior to admission. Moreover, the diagnosis of postoperative COVID-19 as well as isolation and treatment of affected patients remain an important, but complex task. The differentiation of COVID-19 symptoms and those of a normal postoperative course of patients is challenging.

In order to maintain routine thoracic surgery patient care and protect thoracic surgery patients from COVID-19, new strategies in perioperative patient management had to be put in place in March 2020 with no practical experience or data of a similar pandemic available. We describe the implemented measures to protect thoracic surgery patients from postoperative COVID-19 during the 1st and 2nd wave of coronavirus-19 pandemic in Germany and report similarities and differences between symptoms of early COVID-19 and symptoms of patients recovering from thoracic surgery.

Material and methods

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (Ethics Committee of the Ludwig-Maximilians-University of Munich, LMU, Germany, project number 20-618) and with the Helsinki Declaration of 1975, as revised in 2008. This mono-institutional retrospective study was performed at the thoracic surgery, oncological and pneumology departments of the Asklepios Lung Clinic Munich-Gauting, Germany. Informed medical consent was obtained on admission from all patients undergoing thoracic surgery.

Measures to minimize SARS-CoV-2 infections in patients of the thoracic surgery department were analyzed based on internal documentation and validated in our patient cohort. Patient demographic data were retrospectively collected from hospital discharge letters as well as from radiological, histopathological and lung function testing reports. Data of COVID-19 incidence in the district area Munich-Gauting (city of Munich, district of Munich and district of Gauting-Starnberg) and the incidence of whole Germany were obtained from the national platform for geographic data (NPGEO) Corona Hub of the Robert Koch Institute, Germany.

Surgical procedures were performed via video-assisted thoracoscopy or anterolateral thoracotomy under general anesthesia. These procedures included wedge resections, major anatomical resections (segmentectomy, lobectomy, pneumonectomy), pleurectomy, pleurodesis and open tumor biopsies. Minor procedures such as sole chest tube or port catheter placement, cervical lymph node dissection, tracheotomy, vacuum-assisted therapy or bronchoscopy procedures were not included in the study cohort. All patients with benign and malignant disease consecutively admitted for non-elective, semi-elective and elective thoracic surgical procedures between March 1st and May 15th, 2020 were retrospectively included in the study.

With the beginning of the pandemic on March 1st to March 22nd 2020, we experienced three cases of postoperative COVID-19 in detail described in Stoleriu et al., Annals of Thoracic Surgery (2020) [3]. Under the impression of severe disease courses in patients with postoperative COVID-19, we implemented strict prevention measures starting on March 23rd in parallel to the governmental declaration of emergency status in Bavaria, Germany on March 21st. Therefore, the analyzed time frame was subdivided into two time periods: the “Surveillance Phase” from March 1st to March 22nd 2020 and the later “Restriction Phase” from March 23rd to the suspension of the emergency status in Bavaria on May 15th 2020 ([Fig. 1 a]).

Fig. 1 Timeline with regional and national incidence of COVID-19 in Munich-Gauting and Germany, post-operative COVID-19 cases and precautionary measures for postoperative COVID-19 prevention. a Timeline of COVID-19 incidence in whole Germany and in the district area Munich-Gauting with time periods of governmental “lockdown” measures in Bavaria and Germany indicated in green and blue bars. Blue vertical lines indicate dates of surgery of patients with postoperative COVID-19 as in Stoleriu et al. (2020). b Timeline dividing the time interval of interest into a “Surveillance Phase” and a “Restriction Phase” with time periods of preventive measures put in place in the thoracic surgery department of the Asklepios Lung Clinic Munich-Gauting to prevent postoperative COVID-19 during the pandemic.

During the “Surveillance Phase” perioperative patient management and care were performed according to standard operating procedures. The “Restriction Phase” was characterized by implementation of strict preventive measures in the thoracic surgery department to reduce SARS-CoV-2 infections, in parallel with the enactment of governmental regulations, the so-called “lockdown”.

In detail, COVID-19 preventive measures in perioperative patient management were implemented in chronological order, as illustrated in [Fig. 1]: Starting 23rd of March 2020, a standardized pre-admission questionnaire by phone interviews was routinely performed 1–2 days before hospitalization in order to prevent the admission of potentially infected patients and secondary virus transmission. A mouth-nose cover protection became mandatory for all healthcare workers and patients in the hospital. Moreover, SARS-CoV-2 polymerase chain reaction (PCR) from oro-/nasopharyngeal swab was performed in all patients on admission day. Patients were preemptively isolated until a negative PCR test was obtained. Single bedroom accommodation together with a no visitors policy on the normal wards and intensive care unit were introduced. Later, an oro-/nasopharyngeal swab for SARS-CoV-2 PCR was performed in a drive-through setting replacing the testing on admission. In this approach, an out-patient qPCR SARS-CoV-2 screening from oro-/nasopharyngeal swab was performed on the days before admission in a drive-through setting outside the hospital. Following drive-through testing, patients were advised to isolate at home until admission on the next day. Additionally, the incidence of the symptomatic postoperative COVID-19 cases and the clinical characteristics of the affected patients were compared with non-surgical, oncological patients undergoing chemotherapy at the oncological department of the same hospital during the analyzed time interval. The continued surgical patient care during 1st pandemic wave was compared to the same time period (calendar weeks 10–20) of the last 5 years before pandemic. The time between admission and surgery (defined as “time to surgery”), length of hospital stay, as well as the surgical volume were comparatively evaluated before and during 1st and 2nd pandemic waves.

In response to three postoperative COVID-19 cases identified in patients undergoing thoracic surgical procedures during the “Surveillance Phase”, all patients in the “Surveillance Phase” and “Restriction Phase” of the 1st pandemic wave were postoperatively followed-up. Patients were interviewed twice by phone, during the whole early (1st–4th week) and late (5th–8th week) post-discharge phases, in order to depict potential postoperative COVID-19 cases and to determine the incidence of postoperative COVID-19 in our thoracic surgical department. As qPCR tests were nation-wide not available for asymptomatic patients during this time period, this follow-up aimed to identify symptomatic COVID-19 cases only.

In order to identify COVID-19 specific symptoms that only rarely occur during the postoperative course of thoracic surgery patients, we retrospectively compared early symptoms of COVID-19 patients with symptoms of patients recovering from thoracic surgery.

All data are presented as median with interquartile range (1st–3rd quartile). Comparative analysis of patients’ demographics and symptoms between the postoperative surgical cohort (n = 53) and non-surgical COVID-19 patient group (n = 60) was performed by using the Mann-Whitney-U-test for continuous data or the chi-squared test for categorial data, respectively. Statistical differences were considered significant with a type I error rate of p < 0.05. If appropriate, p-values were corrected for multiple-testing using the Bonferroni method. For the three comparisons between the thoracic surgical patient follow-ups and the COVID-19 patient cohort, a Bonferroni factor of 3 was applied, accordingly. Here, only p-values below 0.05/3 = 0.0167 were considered significant ([Table 1]). Statistical analysis was done on Prism version 8.0 (GraphPad, San Diego, CA) and the scikit package version 1.1.0 in Python version 3.6.6.

Table 1 Demographics of patients admitted for thoracic surgery. Demographics are shown for the patient groups in “Surveillance Phase” (March 1st 2020–March 22nd 2020) and “Restriction Phase” (March 23rd 2020–May 15th 2020) of the 1st pandemic wave included in the study.

	“Surveillance Phase” n = 35	“Restriction Phase” n = 54
Age (median [IQR]) years	63 [56–71]	68 [58.8–75.5]
Sex
Female	49 %	35 %
Male	51 %	65 %
BMI (median [IQR]) kg/m2	25 [23] [24] [25] [26] [27]	25 [24–27.5]
Adiposity[*]	14.3 %	11.1 %
Smoker status
Never smoker	14 %	32 %
Ex-smoker	74 %	42 %
Current smoker	11 %	26 %
Pack years (median [IQR])	25 [6–40]	25 [0–40]
Respiratory comorbidities
Asthma/COP	40 %	28 %
Recurrent pneumothoraces	6 %	2 %
Malignant tumors	9 %	6 %
Others	14 %	13 %
Cardiac comorbidities	37 %	28 %
Chronic kidney disease	11 %	15 %
Diabetes mellitus	17 %	15 %
Surgical procedure
Anatomical resection	37 %	43 %
Wedge resection	34 %	26 %
Pleurodesis	34 %	19 %
Others	11 %	20 %
Surgical approach
Thoracoscopy	60 %	44 %
Thoracotomy	40 %	50 %
Others	0 %	6 %
Pathology
Benign disease	31 %	28%
Pleural effusions/pleuritis	14 %	6 %
Hemothoraces	0 %	4 %
Empyema	6 %	6 %
Pneumothoraces	6 %	6 %
Others	5 %	6 %
Malignant disease	69 %	72 %
NSCLC	34 %	35 %
Neuroendocrine lung tumor	0 %	4 %
Pleural mesothelioma	9 %	2 %
Lung metastasis	23 %	22 %
Lymphoma	3 %	0 %
Others	0 %	9 %
Patients with
neoadjuvant	0	2 %
adjuvant chemotherapy	5 %	2 %
adjuvant radiotherapy	0	4 %
adjuvant radiochemotherapy	0	2 %
In-hospital stay
(median [IQR]) days	9 [7] [8] [9] [10] [11] [12]	11.5 [10.0–13.8]

^* Adiposity was defined by a BMI > 30 kg/m² according to the WHO [27].

Results

During the 1st wave of the pandemic, the highest incidence of COVID-19 in Germany and the district area Munich-Gauting ([Fig. 1 a]) was recorded between March 1st and May 15th, 2020. During this time period, 122 surgical procedures were performed in our department. Thirty minor procedures were primarily excluded from the study. Ninety-two procedures were performed on 89 patients and were included in the study. One patient was not admitted for surgery after pre-admission interview due to COVID-19 symptoms and thus not included in the study. The patient was hospitalized for COVID-19 treatment. The surgery was postponed with the patient readmitted for thoracic surgery with two consecutive negative SARS-CoV-2 PCR tests after four weeks. Surgical procedures were postponed in other 4 patients with benign disease in agreement with the patients’ decision. Of note, surgery was offered to additional 7 patients with (suspected) malignant disease and one patient with benign disease, who denied surgery for personal reasons.

Patient demographics are summarized in [Table 1]. Seventy-one to seventy-eight percent of patients reported active nicotine abuse, adiposity, diabetes, respiratory, cardiac or renal comorbidities, seen as risk factors for a severe COVID-19 course of disease. Thirty-five patients underwent surgery in the 22 day long “Surveillance Phase” (in median 11.0 procedures per week), whereas 54 patients underwent surgery during the 54 day long “Restriction Phase” (in median 6.5 procedures per week). Of all 92 surgical procedures performed during both phases, 36 major surgical anatomical resections (34 lobectomies, one segmentectomy and one pneumonectomy) were performed. The remaining surgical procedures included metastasectomies, diagnostic and therapeutic resections of lesions and nodules highly suspicious for malignancy, as well as urgent non-malignant conditions including symptomatic empyemas, pleural effusions, pneumothoraces or hemothoraces.

The number of major surgical procedures during the 1st in comparison to the 2nd pandemic wave as well as prepandemic years (2014–2019) is summarized in Supplementary Table 1S.

The median time to surgery was 2 (1–3) days in the “Surveillance Phase“ and 3 (2–4.8) days in the “Restriction Phase“ of the 1st pandemic wave as well as 1 (1–3) days during the 2nd wave. Similarly, the median time to surgery during the same time interval in 2019 was 1 (1–3) days. Moreover, demographical data did not show any significant differences between the “Surveillance Phase“ and “Restriction Phase“, reflecting a homogenous patient collective in the analyzed periods ([Table 1]).

Three out of 35 patients, who underwent thoracic surgery in the “Surveillance Phase”, were re-hospitalized and diagnosed with COVID-19 pneumonia ([Fig. 1 a], [Fig. 2 a]). Clinical course of these patients was described in detail in Stoleriu et al. (2020) [3].

Fig. 2 Incidence of postoperative COVID-19 with and without pre-admission COVID-19 screening. a Flow chart of 35 patients during the “Surveillance Phase” without pre-admission COVID-19 screening: Three patients with postoperative COVID-19 were identified. b Flow chart of 56 patients during the “Restriction Phase” with pre-admission COVID-19 screening. Two patients tested positive for SARS-CoV-2 from oro-/nasopharyngeal swab and surgery was postponed. In 54 patients who had been tested negative on admission, no postoperative COVID-19 cases were observed.

From 56 patients admitted for surgery in the “Restriction Phase”, two patients tested positive for SARS-CoV-2 preoperatively on admission and were discharged to home quarantine. Both patients were readmitted for the surgery after three and four weeks respectively with two consecutive negative SARS-CoV-2 PCRs from oro-/nasopharyngeal swab. No cases of post-operative COVID-19 were observed during the “Restriction Phase” ([Fig. 2 b]).

Eighty-eight out of 89 surgical patients were followed-up to diagnose symptomatic postoperative COVID-19 after discharge ([Fig. 3]). In three patients operated during the “Surveillance Phase” COVID-19 was ruled out by PCR or computer tomography (CT) upon clinical suspicion ([Fig. 3 a]). Three out of 53 patients in the “Restriction Phase” reported symptoms suspicious for COVID-19 on first follow-up interview and two patients on second follow-up interview. In these patients, COVID-19 was ruled out by two consecutive PCR tests from oro-/nasopharyngeal swab or CT ([Fig. 3 b]).

Fig. 3 Detailed study flow chart showing patients admitted for thoracic surgery during the “Surveillance Phase” and “Restriction Phase”. a In the “Surveillance Phase”, 35 patients underwent thoracic surgery without COVID-19 screening on admission. Three patients were hospitalized for COVID-19 postoperatively. All other patients were followed-up by phone interview, raising suspicion for COVID-19 in other three patients who finally were tested negative by SARS-CoV-2 PCR from oro-/nasopharyngeal swab or CT. b In the “Restriction Phase”, 54 patients underwent thoracic surgery upon negative COVID-19 screening. 53 patients were followed-up in two consecutive phone interviews for COVID-19 typical symptomatology. On 5 occasions clinical suspicion of postoperative COVID-19 based on the patient interviews was made. These patients were followed up by SARS-CoV-2 PCR from oro-/nasopharyngeal swab or CT.

Potential symptoms for COVID-19, such as cough, dyspnea, and low energy levels, also occur during the normal postoperative recovery of thoracic surgery patients. Therefore, the identification of specific symptoms for COVID-19 in this patient cohort might be useful to identify suspected COVID-19 cases and trigger PCR-based COVID-19 testing. We observed a substantial overlap between symptoms of recovering patients after thoracic surgery and potential COVID-19 symptoms, described in literature. Comparing symptoms of patients with confirmed COVID-19 and patients recovering from thoracic surgery, we found that fever, dry cough, dyspnea and diarrhea were significantly more prevalent in patients with COVID-19. Other symptoms such as low energy levels and expectoration appeared similarly frequent in post thoracic surgery patients and in patients suffering from acute COVID-19. Detailed differences in the symptomatology of patients normally recovering from thoracic surgery and COVID-19 patients are summarized in [Table 2].

Table 2 Comparison between symptoms of thoracic surgery patients on postoperative follow-up and acute COVID-19 symptoms. Symptoms reported by patients during recovery from thoracic surgery without COVID-19 approximately 4 weeks (follow-up I) and 8 weeks (follow-up II) postoperatively were compared to those of hospitalized non-surgical COVID-19 patients. For comparisons chi-squared tests were used if not indicated otherwise.

	Thoracic surgery on follow-up I n = 53	Thoracic surgery on follow-up II n = 53	COVID-19 on admission n = 60	follow-up I vs. follow-up II	follow-up I vs. COVID-19	follow-up II vs. COVID-19
Gender (% female)	36 %		45 %	–	p = 0.32
Age (median [IQR])	67 [58–74]		62.5 [51–74]	–	p = 0.18[#]
Fever	2 %	0 %	70 %	p = 0.32	p < 0.001[*]	p < 0.001[*]
Dyspnea	15 %	15 %	48 %	p = 0.99	p < 0.001[*]	p < 0.001[*]
Cough	8 %	11 %	77 %	p = 0.51	p < 0.001[*]	p < 0.001[*]
Diarrhea	13 %	8 %	25 %	p = 0.34	p = 0.11	p = 0.013[*]
Expectoration	13 %	6 %	18 %	p = 0.18	p = 0.46	p = 0.041
Anosmia	8 %	4 %	3 %	p = 0.70	p = 0.32	p = 0.90
Headache	9 %	11 %	13 %	p = 0.75	p = 0.51	p = 0.75
Low energy levels	47 %	35 %	41 %	p = 0.40	p = 0.82	p = 0.40
Body ache	17 %	16 %	25 %	p = 0.99	p = 0.94	p = 0.94
Throat ache	2 %	4 %	2 %	p = 0.56	p = 0.93	p = 0.49
Nausea	11 %	8 %	10 %	p = 0.51	p = 0.82	p = 0.65
Disorientation	5 %	8 %	8 %	p = 0.70	p = 0.58	p = 0.88

^# For comparison of median age, Mann-Whitney-U-test was used.

^* After adjustment for multiple-testing with a Bonferroni factor of 3 as an approximation, only p-values below p < 0.05/3 = 0.0167 were considered significant.

During the same time interval, 398 admissions of oncological patients were recorded in our hospital. In total, 222 patients experiencing malignant lung diseases were primarily admitted for oncological diagnostics (staging examinations, n = 50, 22.5 %), conservative, non-surgical treatment (chemotherapy, n = 132, 59.5 %) or best supportive care (n = 40, 18 %). A pre-admission COVID-19 screening via phone calls was implemented on the oncological department at the same time as in the thoracic surgery department. Three patients undergoing in-hospital chemotherapy (neoadjuvant n = 2, adjuvant n = 1) experienced COVID-19 post-discharge. These patients were systematically followed-up to identify COVID-19 cases, as part of the TERAVOLT study [5]. Taken together, the incidence of symptomatic COVID-19 patients in the analyzed period was 2.3 % upon chemotherapy and 2.5 % upon thoracic surgery. A comparative analysis of patient demographics is illustrated in Supplementary Table 2S.

Conclusion

This study underlines the usefulness of the primary and secondary COVID-19 prevention measures for an uninterrupted patient management and care in the thoracic surgery department of the Asklepios Lung Clinic Munich-Gauting. We report real world data on classical symptomatology of recovering thoracic surgery patients with implications for the screening of postoperative COVID-19. Primary and secondary prevention measures described in this study might serve as blueprint for prevention of postoperative COVID-19, thus ensuring continued surgical treatment of patients with thoracic diseases during the pandemic.

Discussion

The COVID-19 pandemic represents a threat to human health, especially in risk groups such as patients recovering from surgery [6]. Here, we report real world clinical data of thoracic surgery patients during the first COVID-19 wave in Germany from March to May 2020 with focus on the successfully implemented COVID-19 preventive measures that allowed continued care of patients undergoing thoracic surgery.

Previous studies demonstrated the high incidence of complications in patients with postoperative COVID-19. In particular, thoracic surgery patients are prone to severe courses of COVID-19 with postoperative pulmonary complications being associated with a high mortality rate ranging between 27.3–66.7 % [4] [7] [8]. This might be mediated by associated risk factors such as nicotine abuse, cardio-respiratory comorbidities and advanced age in patients suffering from thoracic malignancies, as well as acute lung tissue injury caused by surgery [9]. In accordance with previous studies, the most frequent comorbidities identified in our patients were the pulmonary and cardiac diseases, followed by renal and metabolic comorbidities, suggesting that the admitted surgical patients are often per se high risk patients for severe COVID-19 course – even before surgery. Given the high mortality rate of thoracic surgery patients perioperatively infected with SARS-CoV-2, it is of outmost importance to minimize the spread of the infection in this vulnerable subgroup of patients and to early detect putative symptoms of postoperative COVID-19 [3] [4] [8].

Recommendations of the American Association for Thoracic Surgery and the Thoracic Surgery Outcomes Research Network designed during the first pandemic wave underlined the need for continued surgical care of patients [10] [11], taking the global emergency status of the COVID-19 pandemic and the availability of hospital resources limited by the COVID-19 patient treatment into account. In addition, recommendations of the European Society of Medical Oncology (ESMO) proposed a stage-based lung cancer treatment, with three levels of priority based on clinical, radiological and histological considerations [12]. Subsequently, many surgical departments had to postpone important diagnostic and therapeutic procedures during this challenging time period. As a result, surgical operation volume dramatically decreased in many surgical specialties including vascular, cardiac surgery and general surgery to 28.3 %, 54 % and 57 % of baseline, respectively [13] [14] [15]. A predictive model designed by the COVIDSurg Collaborative, estimated a large amount of surgical operations (ca. 28 mil. for 81.7 % benign and 37.7 % malignant lesions) to be cancelled or postponed worldwide during the first 12 weeks of the pandemic peak in 2020 [16]. Multiple studies showed the medical impact of postponed mandatory diagnostic and surgical procedures [17] [18].

Until March 22nd, three cases of postoperative COVID-19 were identified and triggered the implementation of strict measures to prevent further cases of COVID-19 in thoracic surgical patients. For primary prevention of postoperative COVID-19, the influx of SARS-CoV-2 positive patients into the thoracic surgical departments should be prevented, e. g. by COVID-19 screening measures for admitted patients. In addition, cross-transmission between patients, healthcare workers and visitors should be minimized, e. g. by universal use of nose-mouth covers, no visitors policy and a drive-through approach. During the 1st wave, testing of patients without symptoms was initially not available in test centers. Drive-through testing at our hospital side was initially the only option to test surgical outpatients before admission and aimed to reduce additional hospital rooms for the preoperative COVID-19 screening as well as to overcome a prolonged in-hospital stay. We assume that pre-admission drive-through screening followed by strict home isolation is a feasible approach and equally effective to the in-hospital testing on admission. In addition, pre-admission testing might reduce in-hospital stay time – an important economic factor. Accordingly, the median time to surgery after implementation of the drive-through testing was reduced from 4 to 3 days. With all abovementioned preventive measures took in place, the time to surgery during the 2nd wave was similar in comparison to the last five years.

Furthermore, secondary prevention by early detection of postoperative COVID-19 in surgical patients is of crucial importance to treat these COVID-19 cases early and identify failure of primary prevention measures. This postoperative screening effort was designed to retrospectively identify the potential transmission events on wards and in the operating room [19]. After implementation of the described preventive measures, no perioperative symptomatic COVID-19 cases were identified.

Due to the high prevalence of COVID-19 in the hospital district area, not only patients but also healthcare workers of our department were affected. In the “Restriction Phase”, positive SARS-CoV-2 tests in four symptomatic healthcare workers were reported 8, 14 and 19 days after the surgical procedure of the last COVID-19 patient reported on our department. With permanent surgical mask wearing and no temporal association to the described cases, cross-transmission in the hospital seemed unlikely to us, however, cannot be excluded.

The preventive measures (e. g. single bed accommodation) increased the use of hospital human resources and materials for the admitted thoracic surgery patients and led to lower bed capacity on wards. Accordingly, the surgical routine between March 1st and May 15th, 2020 was not interrupted, but the surgery volume decreased by 23 % compared to the same time frame of the previous six years (2014–2019, data not shown) in our hospital. This might be explained by the implementation of the single bed policy leading to a 50 % reduction of ward capacity in the “Restriction Phase”. In addition, the socio-medical context of the pandemic led also to strict home isolation of multimorbid patients. Consecutively, patient contacts in private medical practices were cancelled or postponed, leading to underdiagnosis of thoracic diseases, such as lung cancer [20].

The abovementioned preventive measures were also applied during the 2nd wave. With no symptomatic postoperative COVID-19 cases reflecting an efficient perioperative prevention, our department reintroduced the standard two-bed rooms policy. These measures led to an increased ward admission capacity and operation volume, with no re-appearance of post-operative COVID-19 cases. Therefore, we believe, that all measures but single-patient room accommodation are helpful to protect patients with no reduction in volume of surgery required.

In order to identify postoperative COVID-19 after discharge, the patients were followed up using standard telephone interviews and symptom-triggered testing of patients. The lack of symptomatic postoperative COVID-19 during the “Restriction Phase” could point at a successful application of the prevention measures. Because of the lack of qPCR tests during the early phase of the pandemic, a qPCR testing from oro-/nasopharyngeal swab was not available for the asymptomatic patients in this study. Thus, the number of asymptomatic post-operative COVID-19 cases remains elusive, being a limitation of the study. However, according to the recently published S2k Guideline-Recommendations for inpatient therapy of patients with COVID-19 (February 2021), only 6 % of the patients with mild symptoms including cough and fever require hospitalization [21]. Based on this consideration, the aforementioned symptoms depicted in the context of the postoperative follow-up by phone calls should trigger SARS-CoV-2 screening. Comparing complaints of surgical patients in postoperative recovery with those of hospitalized COVID-19 patients, several symptoms reported by thoracic surgery patients, such as expectoration, low energy levels and anosmia, were similarly frequently reported by COVID-19 patients. In contrast, symptoms significantly more often seen in COVID-19 patients were fever, dyspnea, cough, and diarrhea. In patients with these postoperative or post-discharge symptoms, COVID-19 should be considered as differential diagnosis and a COVID-19 test should be routinely performed.

Fever and cough were found to be the most prevalent symptoms for a COVID-19 pneumonia [6] [22] [23]. Symptoms found in COVID-19 patients were in accordance with the preliminary description of the COVID-19 symptomatology including fever (83 %), dyspnea (31 %), cough (82 %) and diarrhea (2 %) as initially reported by Chen et al. (2019) [6]. Of note, anosmia was reported in five patients post-thoracic surgery after adjuvant therapy and only in two non-surgical COVID-19 patients, suggesting that this symptom might be considered less helpful in differentiating normal postoperative recovery from postoperative COVID-19. The high prevalence of headache, low energy levels, nausea and disorientation in the thoracic surgery patients postoperatively might also be linked to analgesic treatment or adjuvant chemotherapy. Therefore, these symptoms could be less reliable in screening for postoperative COVID-19. Given the symptom heterogeneity and the course of post thoracic surgery recovery, we assume that it is more challenging to detect a COVID-19 pneumonia in post thoracic surgery patients than in the healthy individuals based on symptomatology.

Based on the successful prevention implemented during the 1st wave and routinely applied in the 2nd wave, we assume that the pre-admission patient interview, the outpatient drive-through PCR screening and the pre-admission home quarantine, might be of long-term benefit and thus, warranty an uninterrupted surgical patient care. Second, our department introduced a weekly screening of healthcare workers prior to vaccination, as well as an immediate screening of patients upon clinical suspicion. Specifically, symptoms including fever, dry cough, dyspnea, or diarrhea should trigger an emergent screening on the wards.

Taken together, the challenges reported on our thoracic surgery department included:

• The lack of first-hand screening experience in the advent of the pandemic that implied a stepwise implementation of primary and secondary preventive measures.

• The abrupt reduction of intensive care resources for the surgical patient care that determined a postoperative monitoring on normal wards.

• The rapid spread of the infection and possible cross-contamination between patients and healthcare workers that emerged a single room patient hospitalization, no visitor policy, as well as mandatory regular screening for patients and healthcare workers or upon clinical suspicion.

• The elusive identification of the asymptomatic postoperative COVID-19 patients in outpatient setting, that determined a second follow up call and a SARS-CoV-2 screening upon clinical suspicion.

Based on these considerations, the lessons learned during the first pandemic wave in our thoracic surgical unit were:

• Continued thoracic surgical patient care was possible in a high-prevalence COVID-19 region by implementing strict primary and secondary preventive measures.

• Symptoms of recovering thoracic surgery patients and COVID-19 patients overlap, complicating COVID-19 diagnosis postoperatively.

• Postoperative dyspnea, fever, cough, or diarrhea in thoracic surgery patients should trigger COVID-19 testing.

Author contributions: R. H., C. K., M. G. S. and K. S. conceptualized the study. M. G. S., M. G., K. S., F. O, J. H., I. K., F. M. S. and N. R. collected and analyzed clinical data and documentation. M. H. N., E. S. P, J. B., U. G., J. K., and N. S. aided in interpreting results. M. G. S. and M. G. drafted and wrote the manuscript. R. H., C. K. and K. S. revised the manuscript. All authors discussed the results and commented on the manuscript.

Competing interests

The authors declare that there is no conflict of interest.

Acknowledgements

We thank all colleagues of the thoracic surgery department, pneumology department, department for infectious diseases and the department for intensive care medicine of the Asklepios Lung Clinic Munich-Gauting for excellent clinical patient care and help with their clinical and scientific expertise. Also, we would like to thank Professor Rudolf Jörres from the Institute and Outpatient Clinic for Occupational, Social and Environmental Medicine, Ludwig-Maximilians-University Munich, Germany for support with his expertise in statistical data analysis.

• References

• 1 Wang D, Hu B, Hu C. et al. Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. JAMA 2020;
• 2 Velavan TP, Meyer CG. The COVID-19 epidemic. Trop Med Int Health 2020; 25: 278-280
• 3 Stoleriu MG, Gerckens M, Hetrodt J. et al. Clinical course of three postoperative symptomatic Covid-19 cases in patients after lung lobectomy. Ann Thorac Surg 2020;
• 4 Nepogodiev D, Bhangu A, Glasbey JC. et al. Mortality and pulmonary complications in patients undergoing surgery with perioperative SARS-CoV-2 infection: an international cohort study. The Lancet 2020; 396: 27-38
• 5 Garassino MC, Whisenant JG, Huang L-C. et al. COVID-19 in patients with thoracic malignancies (TERAVOLT): first results of an international, registry-based, cohort study. Lancet Oncol 2020; 21: 914-922
• 6 Chen N, Zhou M, Dong X. et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet 2020; 395: 507-513
• 7 Huang J, Wang A, Kang G. et al. Clinical course of patients infected with severe acute respiratory syndrome coronavirus 2 soon after thoracoscopic lung surgery. J Thorac Cardiovasc Surg 2020; 160: e91-e93
• 8 Peng S, Huang L, Zhao B. et al. Clinical course of coronavirus disease 2019 in 11 patients after thoracic surgery and challenges in diagnosis. J Thorac Cardiovasc Surg 2020; 160: 585-592.e2
• 9 Sigel K, Wisnivesky JP. Comorbidity Profiles of Patients with Lung Cancer: A New Approach to Risk Stratification?. Ann Am Thorac Soc 2017; 14: 1512-1513
• 10 Antonoff M, Backhus L, Boffa DJ. et al. 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: 601-605
• 11 Moon MR, Jones DR, Adams DH. et al. American Association for Thoracic Surgery: Maintaining the Mission during the COVID-19 Pandemic. J Thorac Cardiovasc Surg 2020;
• 12 Passaro A, Addeo A, von Garnier C. et al. ESMO Management and treatment adapted recommendations in the COVID-19 era: Lung cancer. ESMO Open 2020; 5: e000820
• 13 Hemingway JF, Singh N, Starnes BW. Emerging practice patterns in vascular surgery during the COVID-19 pandemic. J Vasc Surg 2020; 72: 396-402
• 14 Salenger R, Etchill EW, Ad N. et al. The Surge After the Surge: Cardiac Surgery Post-COVID-19. Ann Thorac Surg 2020; 110: 2020-2025
• 15 Riley JS, Luks VL, de Pina LF. et al. COVID-19 Pandemic Significantly Decreases Acute Surgical Complaints. Am Surg 2020; 86: 1492-1500
• 16 COVIDSurg Collaborative. Elective surgery cancellations due to the COVID-19 pandemic: global predictive modelling to inform surgical recovery plans. Br J Surg 2020; 107: 1440-1449
• 17 Moletta L, Pierobon ES, Capovilla G. et al. International guidelines and recommendations for surgery during Covid-19 pandemic: A Systematic Review. Int J Surg 2020; 79: 180-188
• 18 Fligor SC, Tsikis ST, Wang S. et al. Time to surgery in thoracic cancers and prioritization during COVID-19: a systematic review. J Thorac Dis 2020; 12: 6640-6654
• 19 Lai C-C, Shih T-P, Ko W-C. et al. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and coronavirus disease-2019 (COVID-19): The epidemic and the challenges. Int J Antimicrob Agents 2020; 55: 105924
• 20 Maringe C, Spicer J, Morris M. et al. The impact of the COVID-19 pandemic on cancer deaths due to delays in diagnosis in England, UK: a national, population-based, modelling study. Lancet Oncol 2020; 21: 1023-1034
• 21 Kluge S, Janssens U, Welte T. et al. S2k-Leitlinie – Empfehlungen zur stationären Therapie von Patienten mit COVID-19. Pneumologie 2021; 75: 88-112
• 22 Huang C, Wang Y, Li X. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395: 497-506
• 23 Zhou F, Yu T, Du R. et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. The Lancet 2020; 395: 1054-1062
• 24 Nie L, Dai K, Wu J. et al. Clinical characteristics and risk factors for in-hospital mortality of lung cancer patients with COVID-19: A multicenter, retrospective, cohort study. Thorac Cancer 2021; 12: 57-65
• 25 Tian J, Yuan X, Xiao J. et al. Clinical characteristics and risk factors associated with COVID-19 disease severity in patients with cancer in Wuhan, China: a multicentre, retrospective, cohort study. Lancet Oncol 2020; 21: 893-903
• 26 Grasselli G, Greco M, Zanella A. et al. Risk Factors Associated With Mortality Among Patients With COVID-19 in Intensive Care Units in Lombardy, Italy. JAMA Intern Med 2020; 180: 1345-1355
• 27 Sturm R. Increases in morbid obesity in the USA: 2000-2005. Public Health 2007; 121: 492-496

Publication History

Received: 08 March 2021

Accepted: 09 June 2021

Article published online:
14 July 2021