Abstract
Background
This study aims to evaluate the impact of the novel coronavirus disease 2019 (COVID-19) pandemic on cardiac surgery in a single cardiac surgery center in Lithuania.
Methods
Between November 2018 and March 2021, the data of male COVID-19-negative patients (n=81; mean age: 65.5±8.5 years; range, 46 to 87 years) operated during the pandemic were compared with the data of male COVID-19-positive patients operated during the same period (n=14; mean age: 65.2±10.6 years). The number of patiets, demographic and perioperative data were compared between the patients operated during the pandemic (2020/2021 years; pandemic group) and the prepandemic period (2018/2019 years; control group).
Results
A statistically significant difference between the COVID-19-positive and COVID-19-negative patients was found in terms of the frequency of wound infection (n=3, 21.4% vs. n=12, 14.8%; p=0.013), resternotomy due to bleeding (n=2, 14.3% vs. n=0, 0%; p=0.018), and duration of hospitalization after surgery (26.4±20.4 days vs. 15.3±8.9 days; p=0.008). Comparing data of patients who had surgery before and during the pandemic, a significant decrease in the number of cardiac operations (166 vs. 95) was observed. There was significantly increased body mass index (p=0.01) and incidence of diabetes mellitus type 2 (p=0.021) in the pandemic group.
Conclusion
Despite a significantly higher rate of complications in patients infected with COVID-19, planned cardiac surgery with the utilization of adequate protective measures during quarantine is still a better option than a complete cessation of elective cardiac surgery.
Keywords: Cardiac surgery, COVID-19 pandemic, mortality
Introduction
The severe acute respiratory syndromecoronavirus 2 (SARS-CoV-2) outbreak, which was first reported in Wuhan, China in December 2019, has had an enormous worldwide impact.[1] In 2020 March, the World Health Organization (WHO) declared novel coronavirus disease 2019 (COVID-19) as a global pandemic.[2] Until the beginning of September 2021, the laboratories-confirmed cases in Lithuania increased to 292,274 and 4,607 deaths were recorded which main cause was this virus.[3]
Due to the COVID-19 pandemic, an emergency was declared in Lithuania in March 2020, which disrupted the work of the entire healthcare system, reduced the number of planned surgeries, and no exception was the activity in cardiac surgery departments. Similar to all over the world, many heart disease sectors were transformed into COVID-19 departments.[4] This affected the treatment of patients in need of cardiac surgery due to suggestions to delay all elective procedures and focus only on more urgent ones.[5] Most patients waiting for heart surgery were elderly, with chronic lung or heart disease, diabetes, arterial hypertension, or obesity. Therefore, this group of individuals were advised to observe special security during a pandemic, as infection before or after surgery would have been particularly dangerous for them.[6] Also, COVID-19 was associated with respiratory distress, which could significantly increase postoperative patient mortality in complex cardiac surgeries with cardiopulmonary bypass (CPB).[7]
There are limited data about the COVID-19 effect on the survival of patients after cardiac surgery. In addition, there are no precise recommendations for a cardiac surgical patient"s treatment after postoperative COVID-19 diagnosis.
In the present study, we aimed to compare data of COVID-19-positive and COVID-19-negative patients postoperatively operated during the pandemic and to evaluate the impact of pandemic on cardiac surgery patients by comparing the same time periods before and during the pandemic.
Patients and Methods
This retrospective study was conducted at Hospital of Lithuanian University of Health Sciences Kaunas Clinics, Department of Cardiac Surgery between November 2018 and March 2021 The data of postoperatively negative male COVID-19 patients (n=81; mean age: 65.5±8.5 years; range, 46 to 87 years) operated during the pandemic were compared with the data of postoperatively positive male COVID-19 patients operated during the same period (n=14; mean age: 65.2±10.6 years). The clinical course of patients who were COVID-19 positive postoperatively was also evaluated. The number of patients, demographic and perioperative data were compared between patients operated during the pandemic from November 6th, 2020 to February 25th, 2021 (2020/2021 years; pandemic group) and the pre-pandemic period from November 6th, 2018 to February 25th, 2019 (2018/2019 years; control group). Coronary artery bypass grafting (CABG), heart valve and complex (CABG + heart valve) surgeries were performed in these patients. Inclusion criteria were male sex, CABG, valvular and complex operations performed during the selected period. Our study did not involve women, as there were no females infected with COVID-19 during that period. There were no age restrictions in this study. Pre-, peri-, and postoperative patient data, including complications were evaluated.
Quarantine
Under quarantine conditions, various cardiac operations were performed in our hospital. Before a hospitalization, patients were screened for COVID-19. Body temperature, clinical symptoms, and previous contact with those infected with the virus were assessed. For the detection of the SARS-CoV-2 virus, nasopharyngeal samples were taken, and viral ribonucleic acid (RNA) was detected using real-time polymerase chain reaction (PCR). Patients were isolated in special wards, until test results were received. In addition, 72 h before surgical treatment, the PCR test was repeated: in case of a negative result, the patient was operated. After transfer to the department, the patient was PCR-tested with a nasopharyngeal swab every seven days and 48 h before discharge. If the virus infection was detected before surgery, the patient was observed and re-consulted for postponement of cardiac surgery. Healthcare workers and patients always wore protective equipment and relatives were not allowed to visit their family members, except patients who were younger than 14 years old or patients with extremely severe conditions.
All staff were tested according to the procedure established by the Ministry of Health of Lithuania: after contact with the infected person, the staff were re-tested. In case of a positive test result, staff were required to isolate themselves and observe their health condition on an outpatient basis.
Statistical analysis
Statistical analysis was performed using the IBM SPSS version 23.0 software (IBM Corp., Armonk, NY, USA). Continuous data were expressed in mean ± standard deviation (SD), while categorical data were expressed in number and frequency. The differences were checked using the t-test and the Mann-Whitney-Wilcoxon criterion. Differences in categorical variables were checked using the chi-square or the Fisher exact test. Ap value of <0.05 was considered statistically significant.
Results
Postoperative data comparison of Coronavirus-positive and -negative patients
The COVID-19-positive group and the COVID-19- negative groups were similar regarding their baseline characteristics and previous medical history. However, compared to COVID-19 positive group, a higher rate of arterial hypertension was found in the COVID-19 negative group (78.6% vs. 97.5%, p=0.003). Although there was no statistically significant difference, a higher percentage of smokers was spotted in the COVID-19-positive group (35.7% vs. 1 4.8%). I n t he COVID-19-positive group, a statistically significant number of patients required resternotomy due to bleeding. With prolonged treatment due to COVID-19 disease, a higher number of bed days after surgery was observed in the COVID-19-positive group (mean 26.4±20.4 days) (Table 1).
Table 1. Data comparison of postoperatively COVID-19-positive and -negative patients.
| COVID-19 positive (n=14) | COVID-19 negative (n=81) | p | |||||
| n | % | Mean±SD | n | % | Mean±SD | ||
| Before surgery | |||||||
| Age (year) | 67±7.7 | 65.5±8.5 | 0.409 | ||||
| Body mass index (kg/m2) | 29.2±5.4 | 30.3±5.3 | 0.515 | ||||
| Diabetes mellitus type 2 (i nsulin-dependent) | 5 | 35.7 | 27 | 33.3 | 0.862 | ||
| Arterial hypertension | 11 | 78.6 | 79 | 97.5 | 0.003 | ||
| Smoking | 5 | 35.7 | 12 | 14.8 | 0.060 | ||
| Chronic atrial fibrillation | 5 | 35.7 | 19 | 23.5 | 0.330 | ||
| Bed days before surgery | 4±2.8 | 4.5±4.5 | 0.597 | ||||
| Postoperative period: | |||||||
| Glomerular filtration rate (after surgery) | 68±31.8 | 78.5±23.4 | 0.792 | ||||
| Creatinine (mmol/L) (after surgery) | 118.3±61 | 96.5±58.4 | 0.579 | ||||
| Blood transfusions (after surgery) | 5 | 35.7 | 23 | 28.4 | 0.579 | ||
| Resternotomy due to bleeding | 2 | 14.3 | 0 | 0.018 | |||
| Number of bed days after surgery | 26.4±20.4 | 15.3±8.9 | 0.008 | ||||
| Total number of bed days | 30.5±21.1 | 19.8±10.5 | 0.198 | ||||
| Pleural puncture (thoracocentesis) | 3 | 21.4 | 21 | 25.9 | 0.721 | ||
| Pneumonia | 4 | 28.6 | 10 | 12.3 | 0.114 | ||
| Superficial wound infection | 3 | 21.4 | 12 | 14.8 | 0.013 | ||
| Deep wound infection | 2 | 14.3 | 1 | 1.2 | 0.010 | ||
| Paroxysmal atrial fibrillation (I48.0) | 6 | 42.9 | 22 | 27.2 | 0.234 | ||
| Death | 1 | 7.1 | 2 | 2.5 | 0.356 | ||
| SD: Standard deviation; Total bed days: Number of bed days during all stay in hospital. | |||||||
Characteristics and course of the disease in COVID-19-positive patients
Most of the patients were treated with antibiotics. Six patients received specific antiviral treatment. Asymptomatic patients received standard postoperative treatment and their condition was closely observed. Three patients were readmitted to the intensive care unit (ICU) and two patients required reintubation due to COVID-19 infection. Among symptomatic patients, the most common one was fever. Samplings before and after the COVID-19-positivity showed decreased hemoglobin and increased C-reactive protein (CRP), lactate dehydrogenase, and D-dimer levels (Table 2). Only one patient with comorbidities died in that group. This patient became infected 48 days after surgery, although the average time before diagnosing COVID-19 in other patients with this virus was 11 days after surgery. Mediastinitis with sternal wound infection was diagnosed for this patient before COVID-19 infection. His COVID-19 course was complicated with pneumonia and acute respiratory failure.
Table 2. COVID-19-positive patients’ laboratory findings, symptoms, and treatment.
| n | % | Mean±SD | |
| COVID-19 positive patients data | |||
| Time after surgery to COVID-19 diagnosis (days) | 13 | ||
| Amount of time between the last date of laboratory samplings and COVID-19 diagnosis (days) | 1.21 | ||
| White blood cells (X109/L) | 7.9±3.2 | ||
| Neutrophils (%) | 67.2±10.1 | ||
| CRP (mg/L) | 91.1±54.5 | ||
| Hemoglobin (g/L) | 103.2±10.6 | ||
| Symptoms after COVID-19 positive diagnosis: | |||
| Dry cough | 3 | 21.4 | |
| Fever >37.5°C | 9 | 64.3 | |
| Need for oxygen therapy | 6 | 40 | |
| Dyspnea | 4 | 28.6 | |
| No symptoms | 5 | 35.7 | |
| Readmission to ICU | 3 | 21.4 | |
| Reintubation after readmission to ICU | 2 | 14.3 | |
| After COVID-19 positive diagnosis | |||
| Average time of laboratory sampling after COVID-19 diagnosis (days) | 8.75 | ||
| Ferritin (pg/L) | 311.1±345.9 | ||
| Lactate dehydrogenase (U/L) | 350.1±146.8 | ||
| D-dimer (mg/L) | 3±1.4 | ||
| White blood cells (X109/L) | 7±1.8 | ||
| Platelets (X109/L) | 348.1±152 | ||
| Hemoglobin (g/L) | 103.6±8.7 | ||
| CRP (mg/L) | 53.9±54.7 | ||
| Chest computed tomography | 4 | 28.6 | |
| Treatment: | |||
| Remdesivir | 6 | 42.9 | |
| Dexamethasone | 5 | 35.7 | |
| Antibiotics | 9 | 64.3 | |
| Donor plasma with antibodies | 1 | 7.1 | |
| SD: Standard deviation; CRP: C-reactive protein; ICU: Intensive care unit. | |||
Comparison of patients operated before and during the pandemic
The number of patients decreased by double during the pandemic in the same time period: 166 heart surgeries were performed during a 3.5-month period in 2018/2019 years (control group) and only 95 in 2020/2021 (pandemic group) years during the same period. The baseline characteristics of the patients in both groups were similar. However, compared to the 2018/2019 years (control group), patients in the 2020/2021 years (pandemic group) were found to have a higher rate of type 2 diabetes mellitus and higher body mass index (BMI) (Table 3). No statistically significant difference in the duration of surgery, CPB, and cardioplegia time was observed between the two groups in the perioperative period (Table 3).
Table 3. Overall characteristics of patients and their perioperative data comparing (control) and (pandemic) groups.
| 2018/19 years (control) group (n=166) | 2020/21 years (pandemic) group (n=95) | p | |||||
| n | % | Mean±SD | n | % | Mean±SD | ||
| Before surgery | |||||||
| Age (year) | 65.17±10.6 | 65.5±8.5 | 0.762 | ||||
| Body mass index (kg/m2) | 28.1±4.7 | 30.3±5.3 | 0.001 | ||||
| Diabetes mellitus type 2 (insulin-dependent) | 33 | 19.9 | 27 | 33.3 | 0.021 | ||
| COPD | 15 | 9 | 3 | 3.7 | 0.130 | ||
| Smoking | 27 | 16.4 | 12 | 14.8 | 0.755 | ||
| Chronic atrial fibrillation | 30 | 18.2 | 19 | 23.5 | 0.330 | ||
| Bed days before surgery | 6±5.4 | 4.5±4.5 | 0.017 | ||||
| Perioperative period | |||||||
| Urgent surgery | 7 | 4.2 | 7 | 8.6 | 0.158 | ||
| Elective surgery | 149 | 89.8 | 71 | 87 | 0.619 | ||
| Emergency surgery | 10 | 6 | 3 | 3.7 | 0.443 | ||
| CABG | 97 | 58.4 | 50 | 61.7 | 0.620 | ||
| CABG + valve surgery | 35 | 21.1 | 16 | 19.8 | 0.808 | ||
| Valve surgery | 30 | 18.1 | 15 | 18.5 | 0.932 | ||
| Cardiac arrest time (min) | 56.7±24.2 | 60±27.9 | 0.351 | ||||
| SD: Standard deviation; COPD: Chronic obstructive pulmonary disease; CABG: Coronary artery bypass grafting. | |||||||
Discussion
To prevent COVID-19 outbreaks in hospitals, the units had particularly stricter staff and patient screening. The United Kingdom (UK) paid particular attention to the followings: all patients were tested for COVID-19 before surgery, staff used personal protective equipment, the floors, where infected and non-infected patients were treated, were separated, and staff rotation was as infrequent as possible to reduce the likelihood of virus transmission.[8] Similar measures were applied in Lithuanian hospitals, as well. However, although the hospital departments strictly adhered to the National Public Health Center (NPHC) instructions and recommendations (i.e., temperature measurements, epidemiological verification, personal protective equipment), the spread of the virus could not be completely prevented. The COVID-19 infections among staff and patients after surgeries were recorded in the cardiac surgery unit of our hospital.
Although several studies have demonstrated that the incidence of COVID-19 infection may be associated with diabetes, higher European System for Cardiac Operative Risk Evaluation (EuroSCORE II), higher preoperative serum creatinine levels,[9] BMI[10] and age,[11] there were no s tatistically significant differences in our study comparing COVID-19 infected and non-infected patients.
Furthermore, our study involved only men, as there were no females infected with COVID-19 during the study period. As reported in the literature, there is no significant difference in the proportion of males and females with confirmed COVID-19 diagnosis.[12] The lack of female patients in our study can be explained by the fact that women accounted for a smaller proportion of cardiac surgical patients, and probably as they were more obligated to adhere to anti-pandemic requirements. Another possible cause is the spread of the virus in the postoperative wards, which are different for men and women.
As the preoperative data of patients with and without COVID-19 who underwent surgery in 2020/2021 was similar, it can be concluded that patients became infected with COVID-19 regardless of their health condition and comorbidities. A higher percentage of smokers in the COVID-19- positive group can be related to the increased contamination due to repetitive hand interactions with the mouth during smoking process and higher number of contacts without wearing a mask. Also, smoking can change angiotensin-converting enzyme 2 (ACE-2) gene expression and cause immune system weakening.[13] In the COVID-19-positive group, a statistically significant number of patients required resternotomy due to bleeding. Other studies have shown that the most likely pathophysiological mechanism causing bleeding after surgery is CPB-related inflammatory reaction. The CPB may exacerbate the harmful effect of COVID-19 on the coagulation system. Therefore, cardiac surgery patients with postoperative COVID-19 appear to be more susceptible to postoperative bleeding requiring surgical revision.[14] Increased bleeding in the COVID-19-positive group may have led to a higher rate of wound infections. On the other hand, comparing the rate of complications in both groups, similar results were obtained.
Although a statistically higher mortality rate was found in similar studies carried out in other countries,[9,15] there was no statistically significant difference in mortality between COVID-19-positive and COVID-19-negative patients in our study.
Moreover, the patient's condition and symptoms after cardiac surgery can be very similar to COVID-19 disease (temperature, shortness of breath). Blood sampling results such as an increase of lactate dehydrogenase, CRP, and D-dimer may help to suspect patients to be infected with virus.[16] Our study also showed that patients who were infected with the virus had an increase in these laboratory sampling results. This finding suggests that there is a correlation between these blood samplings and COVID-19 infection. In case of suspicion, it would be wise to have a nasopharyngeal swab test immediately.
E valuating the data of cardiac surgery patients operated in our hospital, the impact of COVID-19 on the number of surgeries was observed. Twice fewer patients in 2020/2021 underwent surgery compared to the same period before the pandemic, due to quarantine restrictions and decreased medical support availability due to COVID-19 virus. Decreased number of surgeries due to the pandemic was also observed in other countries. In the UK and Israel, all planned surgeries were canceled, only emergency and urgent cardiac surgeries were performed.[8,15] There are no exact data in the literature on what happened to those patients who did not have planned heart surgery, but negative effects of delayed operations are described in the literature.[17,18] Despite quarantine restrictions, a relatively large amount of elective surgery was performed in our hospital. However, all patients were selected and surgeries were performed only in case of patient's worsening state. In the current study, we examined what happened to patients operated during the pandemic and whether it was safe to do so.
General characteristics and perioperative data did not significantly differ between the control and pandemic groups, and similar results were obtained in other studies.[15,17] However, the slower pace of l ife showed a statistically significant increase in patients" BMI during quarantine (p=0.001), and more patients from the pandemic group had type 2 diabetes mellitus, which may have contributed to a longer duration of hospitalization.
Although at the time of writing this report, around 70% of the country's population have been vaccinated, face protection and special clothing sets are used in the departments in case of contact with a potentially infected person or confirmed case. We believe that this and the other measures listed above reduce the number of COVID-19 infections in the hospital setting. Other authors have also reported similar findings.[19] Quarantine restrictions lead to longer patients waiting lists for elective and emergency cardiac and thoracic surgeries. While preparing for surgical interventions, special attention should be paid to the care of elderly patients with cardiovascular disorders. Thus, decisions regarding the surgical treatment of patients must be made by a multidisciplinary team consisting of cardiovascular and thoracic surgeons, as well as experts in vaccination, geriatrics, pulmonology, and virology.[20]
The main limitation to this study is that the sample size of the COVID-19-positive group is small (n=14); however, this relatively small sample size also indicates that the protective measures used were quite effective.
The main strength of this study is that the control group data were used to assess the effect of the pandemic, which is lacking in many other similar studies. It should also be considered an advantage to provide data, when the clinic has not stopped elective cardiac surgery, as in many cardiac surgery clinics in other countries. In addition, we were able to analyze pre-vaccination data. We do not consider the findings to be less relevant, as some patients still refuse vaccination and some vaccinated or relapsed individuals develop COVID-19 again.
In conclusion, although postoperative mortality did not differ between COVID-19-positive and COVID-19-negative groups, hospitalization for COVID-19-positive patients lasted longer. They were also more likely to undergo resternotomy for bleeding with a higher incidence of wound infection. The number of cardiac surgery operations performed during the pandemic decreased by half in our hospital and COVID-19 was detected in some of our patients postoperatively despite protective measures. Planned cardiac surgery during the COVID-19 pandemiccaused quarantine seems to be better for the patient than a complete cessation of elective cardiac surgery, if adequate protective measures are taken.
Footnotes
Conflict of Interest: The authors declared no conflicts of interest with respect to the authorship and/or publication of this article.
Author Contributions: Idea/Concept: A.B., L.J.; Design: V.V., A.B.; Control/supervision: A.B., P.J., E.R., L.J.; Data collection and/or processing: V.V., M.K., K.K.; Analysis and/or interpretation: V.V., A.B.; Literature review: V.V., M.K., K.K.; Writing the article: V.V., A.B., M.K., K. K.; Critical review: A.B., P.J., E.R., L.J.; References and fundings: V.V., A.B., M.K., K.K.
Financial Disclosure: The authors received no financial support for the research and/or authorship of this article.
References
- 1.Gunaydin S, Stammers AH. Perioperative management of COVID-19 patients undergoing cardiac surgery with cardiopulmonary bypass. Perfusion. 2020;35:465–473. doi: 10.1177/0267659120941341. [DOI] [PubMed] [Google Scholar]
- 2.Soetisna TW, Buana AC, Tirta ES, Ardiyan A, Aligheri D, Herlambang B, et al. A 48-year-old man at low risk for SARS-CoV-2 infection who underwent planned elective triple-vessel coronary artery bypass graft surgery at a National Heart Center in Indonesia followed by a fatal case of COVID-19. e928900Am J Case Rep. 2021;22 doi: 10.12659/AJCR.928900. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Praėjusios paros statistika - Oficialiosios statistikos portalas. 2021. Available at: https://osp.stat.gov.lt/praejusios-paroscovid-19-statistika .
- 4.Bonalumi G, di Mauro M, Garatti A, Barili F, Gerosa G, Parolari A; Italian Society for Cardiac Surgery Task Force on COVID-19 Pandemic. The COVID-19 outbreak and its impact on hospitals in Italy: The model of cardiac surgery. Eur J Cardiothorac Surg. 2020;57:1025–1028. doi: 10.1093/ejcts/ezaa151. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Fukuhara S, Rosati CM, El-Dalati S. Acute type A aortic dissection during the COVID-19 outbreak. e405-e407Ann Thorac Surg. 2020;110 doi: 10.1016/j.athoracsur.2020.04.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Haft JW, Atluri P, Ailawadi G, Engelman DT, Grant MC, Hassan A, et al. Adult cardiac surgery during the COVID-19 pandemic: A tiered patient triage guidance statement. Ann Thorac Surg. 2020;110:697–700. doi: 10.1016/j.athoracsur.2020.04.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Asimakopoulos G, Smith PL, Ratnatunga CP, Taylor KM. Lung injury and acute respiratory distress syndrome after cardiopulmonary bypass. Ann Thorac Surg. 1999;68:1107–1115. doi: 10.1016/s0003-4975(99)00781-x. [DOI] [PubMed] [Google Scholar]
- 8.Balmforth D, Yates MT, Lau K, Hussain A, Lopez-Marco A, Edmondson S, et al. Cardiothoracic surgery in the midst of a pandemic: Operative outcomes and maintaining a coronavirus disease 2019 (COVID-19)-free environment. JTCVS Open. 2020;4:107–114. doi: 10.1016/j.xjon.2020.09.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Keizman E, Ram E, Kachel E, Sternik L, Raanani E. The impact of COVID-19 pandemic on cardiac surgery in Israel. J Cardiothorac Surg. 2020;15:294–294. doi: 10.1186/s13019-020-01342-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Nader J, Anselmi A, Tomasi J, Martin A, Aymami M, Rouze S, et al. Adult cardiac surgery during COVID-19 lockdown: Impact on activity and outcomes in a high-volume centre. Arch Cardiovasc Dis. 2021;114:364–370. doi: 10.1016/j.acvd.2020.12.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Byrnes ME, Brown CS, De Roo AC, Corriere MA, Romano MA, Fukuhara S, et al. Elective surgical delays due to COVID- 19: The patient lived experience. Med Care. 2021;59:288–294. doi: 10.1097/MLR.0000000000001503. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Sanders J, Akowuah E, Cooper J, Kirmani BH, Kanani M, Acharya M, et al. Cardiac surgery outcome during the COVID-19 pandemic: A retrospective review of the early experience in nine UK centres. J Cardiothorac Surg. 2021;16:43–43. doi: 10.1186/s13019-021-01424-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Garg S, Kim L, Whitaker M, O'Halloran A, Cummings C, Holstein R, et al. Hospitalization rates and characteristics of patients hospitalized with laboratory-confirmed coronavirus disease 2019 - COVID-NET, 14 states, March 1-30, 2020. MMWR Morb Mortal Wkly Rep. 2020;69:458–464. doi: 10.15585/mmwr.mm6915e3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Li X, Xu S, Yu M, Wang K, Tao Y, Zhou Y, et al. Risk factors for severity and mortality in adult COVID-19 inpatients in Wuhan. J Allergy Clin Immunol. 2020;146:110–118. doi: 10.1016/j.jaci.2020.04.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Gülsen A, Yigitbas BA, Uslu B, Drömann D, Kilinc O. The effect of smoking on COVID-19 symptom severity: Systematic review and meta-analysis. Pulm Med. 2020;2020:7590207–7590207. doi: 10.1155/2020/7590207. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Peckham H, de Gruijter NM, Raine C, Radziszewska A, Ciurtin C, Wedderburn LR, et al. Male sex identified by global COVID-19 meta-analysis as a risk factor for death and ITU admission. Nat Commun. 2020;11:6317–6317. doi: 10.1038/s41467-020-19741-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Chiariello GA, Bruno P, Pavone N, Calabrese M, D'Avino S, Ferraro F, et al. Bleeding complications in patients with perioperative COVID-19 infection undergoing cardiac surgery: A single-center matched case-control study. J Cardiothorac Vasc Anesth. 2022;36:1919–1926. doi: 10.1053/j.jvca.2021.11.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Mardani R, Ahmadi Vasmehjani A, Zali F, Gholami A, Mousavi Nasab SD, Kaghazian H, et al. Laboratory parameters in detection of COVID-19 patients with positive RT-PCR; a diagnostic accuracy study. e43Arch Acad Emerg Med. 2020;8 [PMC free article] [PubMed] [Google Scholar]
- 19.Mavioğlu HL, Ünal EU, Aşkın G, Küçüker ŞA, Özatik MA. Perioperative planning for cardiovascular operations in the COVID-19 pandemic. Turk Gogus Kalp Dama. 2020;28:236–243. doi: 10.5606/tgkdc.dergisi.2020.09294. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Donatelli F, Miceli A, Cirri S, Coscioni E, Napoli C. COVID-19 and the second wave during autumn: Preventive strategies in cardiac and thoracic surgery divisions. Eur Surg. 2021;53:37–39. doi: 10.1007/s10353-020-00682-9. [DOI] [PMC free article] [PubMed] [Google Scholar]