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ORIGINAL ARTICLE
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Clinical presentation and course of the novel coronavirus disease 2019 in patients with various types of cancer: A retrospective case–control analysis of an experienced cancer center in Turkey


1 Department of Medical Oncology, University of Health Sciences, Gulhane School of Medicine, Ankara, Turkey
2 Department of Infection Disease, University of Health Sciences, Gulhane School of Medicine, Ankara, Turkey
3 Department of Urology, Nevsehir Government Hospital, Nevsehir, Turkey
4 Department of Radiology, University of Health Sciences, Gulhane School of Medicine, Ankara, Turkey
5 Department of Internal Medicine, University of Health Sciences, Gulhane School of Medicine, Ankara, Turkey
6 Department of Anesthesiology, University of Health Sciences, Gulhane School of Medicine, Ankara, Turkey
7 Department of Intensive Care Unit, University of Health Sciences, Gulhane School of Medicine, Ankara, Turkey
8 Department of Chest Disease, University of Health Sciences, Gulhane School of Medicine, Ankara, Turkey
9 Department of Biochemistry, University of Health Sciences, Gulhane School of Medicine, Ankara, Turkey

Date of Submission28-May-2020
Date of Decision16-Jul-2020
Date of Acceptance21-Jul-2020
Date of Web Publication21-Jan-2021

Correspondence Address:
Ramazan Acar,
Department of Medical Oncology, University of Health Science, Gulhane School of Medicine, Etlik, Kecioren, Ankara
Turkey
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcrt.JCRT_715_20

 > Abstract 


Objective: Cancers have been reported to worsen the clinical course of coronavirus disease 2019 (COVID-19) infection. We aimed to demonstrate the real-life data on health outcomes in COVID-19-infected cancer patients.
Materials and Methods: We analyzed the data of 43 COVID-19-infected cancer patients in our COVID-19 clinics between March 25, 2020, and May 9, 2020, retrospectively.
Results: We determined that 1051 patients were followed up with COVID-19 infection and 43 (4%) of them were cancer patients. The mean age of the patients was 64.3 ± 12.3 years. Lung cancer is the most common cancer type among the patients (23.2%). Dyspnea (51.2%) was the most common symptom in the first admission. Typical ground-glass consolidation or patchy appearance with peribronchial thickening resembling bronchopneumonia on high-resolution computed tomography (HRCT) was present in 29 (67.4%) patients. COVID-19 was diagnosed in 14 (32.5%) patients based on reverse transcriptase-polymerase chain reaction analysis of nose-throat swab samples without any sign of lung involvement on HRCT. Total mortality of the COVID-19 infection was 46.5% (n = 20). Presence of heart disease (hazard ratio [HR]: 3.5; 95% confidence interval [CI]: 1.29–9.4), previous surgeries to the respiratory system (HR: 6.95; 95% CI: 1.29–27.7), and presence of dyspnea at admission (HR: 4; 95% CI: 1.31–12.3) were statistically significantly associated with death (P = 0.01, 0.02, and 0.01, respectively).
Conclusion: Our practices supported that cancer patients were more affected by COVID-19 disease than the normal population. However, our findings can not be generalized due to being retrospective and single centered study, Also, we did not compare the findings with noncancer patients with COVID19 disease.

Keywords: Cancer, coronavirus disease 2019, mortality



How to cite this URL:
Acar R, Yilmaz G, Savasci U, Aykan MB, Kiziloz H, Cuce F, Kadioglu E, Filiz M, Fidan G, Eksert S, Taskin G, Dogan D, Arslan Y, Tasci C, Kayahan N, Dogan T, Basgoz BB, Sertoglu E, Erturk I, Keskin GS, Okcelik S, Yildiz B, Karadurmus N. Clinical presentation and course of the novel coronavirus disease 2019 in patients with various types of cancer: A retrospective case–control analysis of an experienced cancer center in Turkey. J Can Res Ther [Epub ahead of print] [cited 2021 Mar 4]. Available from: https://www.cancerjournal.net/preprintarticle.asp?id=307512




 > Introduction Top


In the last months of 2019, a new coronavirus, which first appeared in Wuhan, China, and attracted attention with its pneumonia in the foreground, was identified. It has been defined as “COVID-19” as an abbreviation of coronavirus disease that appeared in 2019, by the World Health Organization (WHO). The virus, which causes COVID-19 disease and mainly severe respiratory syndrome, has been named as “severe acute respiratory syndrome-coronavirus-2.”[1] COVID-19 virus spread rapidly and unexpectedly all over the world. As of May 23, 2020, the WHO reported 5.1 million cases worldwide. It has been reported that >333,400 people died among these cases.[2] The first case by the Ministry of Health of the Republic of Turkey was proclaimed in March 2020. Turkey's total confirmed cases stood at 154,500, according to the data shared by the Ministry of Health on May 23, 2020.[3]

Diseases that are thought to increase the morbidity and mortality of COVID-19 infection include cardiovascular diseases, diabetes, hypertension (HT), chronic lung diseases, chronic kidney failure, and cancers[4],[5] In particular, hematological and lung cancers and all metastatic cancers have been reported to worsen the clinical course of COVID-19 infection.[6] According to a recently reported publication, 6% of all COVID-19 cases in New York City are cancer patients.[7] In sum, cancer patients have been identified as a highly sensitive group. These cases need to be handled with the utmost care.

During this period, the experiences of various centers on COVID-19 infection in patients with cancer have been reported recently.[7],[8] In our country, as far as we know, a comprehensive statement has not been made yet.

In this study, we aimed to evaluate admission symptoms, clinical features, and the factors affecting the prognosis of cancer patients who were followed up in a tertiary hospital for COVID-19 infection.


 > Materials and Methods Top


Study design and cases

The study was carried out by investigating patients with various types of solid and nonsolid tumors who have been treated and/or currently under treatment in the University of Health Sciences, Gulhane Research and Training Hospital, from March 25 to May 9 in COVID-19 diagnosis, follow-up, treatment, complications, and infection-related outcomes. Patients' medical records were evaluated after obtaining the approval of the institutional ethics committee and the Turkey Ministry of Health. COVID-19-suspected patients were enrolled based on not only the clinical appearance but also the suspicious radiologic findings and/or laboratory-confirmed COVID-19 results collected from the nasal or pharyngeal swab samples.

Statistical analysis

Medical records of suitable cases were enrolled in a SPSS Statistics for Windows (v15.0; IBM Corp, Chicago, IL., USA) datasheet by the registered staff of the Department of Oncology at the University of Health Sciences.

Descriptive information of the study group was presented in mean with standard deviation or median with interquartile range (IQR), where appropriate, depending on the normality of the distribution. Shapiro–Wilk test was conducted for testing the normality of distribution. For the binominal data, a Pearson's Chi-squared test was utilized for the same purpose. Student's t-test and Mann–Whitney U-test were also used for the comparison of the independent variables, where appropriate. Kaplan–Meier survival tables and plots were provided. A Cox regression model with hazard ratio (HR) was conducted to investigate the suspected interfering factors which may alter the survival outcomes. A confidence interval (CI) within 95% was considered for implementing the statistical analysis. P < 0.05 was considered statistically significant. SPSS 15.0 (Chicago, IL, USA) was used for data collection and analyses.


 > Results Top


Demographic and clinical characteristics

It was determined that 1051 patients were followed up with COVID-19 infection between March 25, 2020, and May 9, 2020. Forty-three (4%) COVID-19-infected cancer patients were observed. The mean age of the patients and median length of stay in the hospital were 64.3 ± 12.3 years and 9 days (IQR: 5–12), respectively. The demographic and clinical and oncologic features are listed in [Table 1].
Table 1: Demographic and clinical features

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Lung cancer is the most common cancer type among the patients included in the study. Lymphoid malignancies and colon cancer were the other most common types of cancer. The distribution of the detected cancer types is reported in [Table 1]. A significant proportion of the patients were followed up as Stage 4 disease (51.1%). All patients had anti-neoplastic therapy in their history. Twenty patients (46.5%) who were included in the study at the beginning of the pandemic were still under ongoing chemotherapy program. Eight (18.6%) of these patients used hormonal agents for prostate cancer and breast cancer. Sixteen patients received chemotherapy within 14 days before being diagnosed with COVID-19. During the outbreak, two patients were found to have received radiotherapy. One of these patients had received radiotherapy to the mediastinal area. Only one patient was found to have received immunotherapy before getting a diagnosis of infection. Due to the COVID-19 infection, a total of 23 patients' cancer treatment was delayed or had to be interrupted. Lung metastasis was present in 6.9% of the patients. Nearly 4.6% of the patients had a previous lung surgery. The most common additional comorbidity in all patients was determined as HT (55.8%). The majority of patients were still smokers or smoked beforehand (18.6% and 48.8%, respectively). Angiotensin-converting enzyme (ACE) inhibitors and angiotensin receptor blockers (ARBs) were the most common noncancerous treatment modalities in the entire group (20.9% and 30.2%, respectively).

Dyspnea (51.2%) was the most common symptom in the first admission of patients included in the study. Cough and fever were the other most common symptoms (37.2% and 34.9%, respectively). In our patient group, no symptoms such as anosmia or taste disturbance were detected. All data about symptoms are presented in [Table 2].
Table 2: Symptoms, treatments, and clinical outcomes

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It was found that three of the patients included in the study had COVID-19 infection in their families. One of these patients was followed up at the intensive care unit (ICU). However, no deaths were observed in any patient or family member.

Findings on laboratory and radiology

According to baseline laboratory results, seven (16.2%) patients presented with anemia (hemoglobin [Hb] <10 g/dL). In terms of neutrophil, lymphocyte, and thrombocyte counts, two patients were in severe neutropenia <100/mL and lymphopenia <100/mL, however, prominent neutrophilia and lymphocytosis (>8000 and >4800/mL) were present in 14 and 1 patients, respectively. Thrombocyte count was within normal range in 31 patient >150×103/mm3, although two were in remarkable thrombocytopenia and one in severe condition (<10×103/mm3). Erythrocyte sedimentation rate and C-reactive protein (CRP) levels were mostly elevated ranging from 10 to 133 for sedimentation and from 5 to 357 for CRP. Albumin levels were lower than normal in five (11.6%) patients and lactate dehydrogenase (LDH) levels were higher than normal range in 23 patients (53.4%). D-dimer level had elevated in 22 patients (51.1%). The details of other biochemical indices are shown in [Table 3].
Table 3: Laboratory results

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Typical ground-glass consolidation or patchy appearance with peribronchial thickening resembling bronchopneumonia on high-resolution computed tomography (HRCT) was present in 29 (67.4%) patients. Bilateral pulmonary involvement was present in 22 patients (51.6%). Single or multiple pulmonary metastases were complicated with COVID-19 lung involvement, which were detected on HRCT in three patients. COVID-19 was diagnosed in 14 patients (32.5%) based on reverse transcriptase-polymerase chain reaction (RT-PCR) analysis of nose-throat swab samples without any sign of lung involvement on HRCT. Samples of HRCT sections demonstrating the lung involvement are depicted in [Figure 1], [Figure 2], [Figure 3], [Figure 4].
Figure 1: The patient was a 70-year-old male; he had been treated as Stage 2 colon cancer. He was diagnosed as coronavirus disease 2019 with polymerase chain reaction test. (a-c) Noncontrast thorax computed tomography axial plane images showing active infiltrations with bilateral lower lobes; peripheral-weighted, frosted glass densities (filled arrows); and halo sign (thin arrow) lesions. (d and e) Two weeks later, control computed tomography showed that the lesions in previous computed tomography turned into homogeneous hyperdense consolidations, with traction bronchiectasis (arrows) inside them and parenchymal distortion around them. (f) Subpleural lines (arrow) accompanied

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Figure 2: The patient was a 64-year-old male. He had been treated as Stage 4 gastric cancer since December 2018. He was diagnosed as coronavirus disease 2019 disease with tomography findings. He had negative coronavirus disease 2019 chain reaction test. He died on the 3rd day after diagnosis. (a and b): Noncontrast thorax computed tomography axial plane images showing densities of active infiltrations in both lungs, in a multifocal, frosted glass, and crazy paving pattern (arrows). The findings were frequently reported in coronavirus disease parenchymal involvement

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Figure 3: The patient was a 61-year-old female. She had been treated as Stage 3 non-Hodgkin lymphoma and was diagnosed as coronavirus disease 2019 on polymerase chain reaction test (a) Noncontrast thorax computed tomography axial plane images showing active infiltrations in the right lower lobe with peripheral, ground-glass density (arrow) (b) On computed tomography after 3 days, new consolidations (thin arrow) were observed in the left lower lobe periphery, where the ground-glass density areas in the previous computed tomography progressed to the consolidation (filled arrow) pattern. (c and d) New infiltrations were present as ground-glass density (arrow) compared to the previous computed tomography

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Figure 4: The patient was a 76-year-old male. He had been treated as Stage 4 non-Hodgkin lymphoma since September 2019. He was diagnosed as coronavirus disease 2019 on polymerase chain reaction test and had no coronavirus disease 2019 polymerase chain reaction-positive family history. (a and b) Noncontrast thorax computed tomography axial plane images showing bilateral lower lobes, with densities of diffuse (filled arrow) and round shaped (thin arrow), containing air bronchograms

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Treatment modalities and course of events

After the initial evaluation, 22 (51,1%) patients were discharged to be self-quarantined at home after spending at least two nights in the hospital ranging from 2 days to 22 days, however 21 (48.8%) patients were eventually deteriorated and required ICU care. Among the hospitalized patients, the median length of stay in the hospital was 8.5 days (IQR: 3–13.7). All patients received nasal oxygen therapy when needed, although eventually 17 were in need of mechanical ventilation and intubation. Four patients were treated with nasal oxygen or noninvasive pressurized ventilators, when required, in the ICU. A broad-spectrum antibacterial therapy was administered in 35 (81.3%) patients including 3rd-generation cephalosporins, teicoplanin, anti-pseudomonal azlo-ureido penicillin, carbapenems, linezolid, and macrolides for empirical purpose. All patients received a low-molecular-weight heparin for thromboprophylaxis. Chloroquine, a common antimalarial and anti-rheumatism drug, was used in forty (93%) patients. Moreover, other wishfully effective antiviral agents including oseltamivir, favipiravir, and azithromycin which is also a macrolide antibacterial were used solely or in combination with chloroquine or other antiviral agents in 20 (46.5%), 19 (44.2%), and 22 patients (51.2%), respectively. An immune plasma exchange was done in one patient [Table 2].

Total leukocyte count, CRP, creatine kinase-muscle brain (CK-MB), troponin, LDH, and ferritin at admission were significantly higher in patients who needed treatment in the ICU where Hb levels; neutrophil, lymphocyte, and thrombocyte counts; sedimentation rates; and D-dimer and CK levels were similar. In addition, albumin levels were statistically significantly lower in those who were followed in the ICU (P = 0.02). Comparisons of the laboratory results between patients hospitalized after self-quarantined at home and ICU-required patients are summarized in [Table 2].

For patients who were followed up in the ICU, the median length of stay in the hospital, length of stay in the ICU, and duration of intubation with mechanical ventilation were 7 (IQR: 3–12.7), 5 (IQR: 1.25–7), and 3 (IQR: 1–5.75) days, respectively. Up till now, May 10, 2020, one patient had been fully recovered, whereas 4 are still under treatment, 16 died in the ICU, and 2 more died at the clinic in self-quarantine. The course of events and details is described in footnotes in [Table 2].

The total mortality of the COVID-19 infection in the study group was 46.5% (n = 20). The median survival was 13 days (95% CI: 7.6–18.3) and 10-day survival rate was 65.5%. On univariate analyses utilizing Cox regression model, presence of heart disease including congestive heart disease, coronary artery disease, and atrial fibrillation (HR: 3.5; 95% CI: 1.29–9.4); previous surgeries to the respiratory system (lobectomy) (HR: 6.95; 95% CI: 1.29–27.7); and presence of dyspnea at admission (HR: 4; 95% CI: 1.31–12.3) were statistically significantly associated with death (P = 0.01, P = 0.02, and P = 0.01, respectively). In addition, invasive mechanical ventilation and intubation were linked to less survival outcomes (HR: 2.75; 95% CI: 1.02–7.46, P = 0.045) [Figure 5]. Use of AT receptor inhibitors was slightly related to a better survival outcome and contrarily presence of suspicious initial HRCT findings for COVID-19 was slightly related to worse outcome, those of which were not statistically significant (P = 0.06 and P = 0.06, respectively). The association of clinical factors with worse survival outcomes is summarized in [Table 4]. On multivariate analysis, none of the factors were associated with survival outcome, with an annotation for dyspnea at admission showing a borderline significance (P = 0.06).
Figure 5: (a-c) Kaplan–Meier curves of risk factor for mortality

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Table 4: Factors affecting survival based on univariate analysis in patients with COVID-19

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 > Discussion Top


As it is known, COVID-19 has influenced the whole world under all aspects. All patients with chronic illness, including cancer, were adversely affected by the pandemic.[9] COVID-19 increased the risk due to the effects of both treatment modalities and tumor burden on the immune system during cancer treatment. Like all centers, we created our own approach according to our real-life data with European Society for Medical Oncology and American Society of Clinical Oncology guidelines in this time period.[10] All cancer patients admitted in our hospital were evaluated in coordination with the COVID-19 management unit. By making a patient-based decision, we continued the treatment of some patients as before. In other patients, we developed alternative approaches within the recommendation of the guidelines. Since the beginning of the pandemic, patients diagnosed with COVID-19 in our tertiary health center have been treated according to the literature.[11] Among these patients, there are 43 cancer patients. Our results showed that 65% of the patients were male. Lung, lymphoma, and colon cancers were the most common cancer types. Nearly 79% of the patients had Stage 3 and Stage 4 diseases. Almost 72% of them were still receiving cancer treatment at the time when COVID-19 was diagnosed. Almost all of them had HT, diabetes mellitus (DM), coronary heart disease (CHD), and chronic obstructive pulmonary disease (COPD) as comorbid diseases. The average age of the patients was 64.3 years. Most of the patients were in the geriatric age group. Approximately 68% of them had a smoking history. Nearly 53% of them had a history of ACE inhibitor, ARB, and ibuprofen use. Given all the features, we found in our study group that it is obvious that they pose a great risk for COVID-19.[6] In our patient group, twenty (46.5%) patients died due to COVID-19 infection. Zhang et al. reported 28 COVID-19-infected cancer patients' clinical features and outcomes. Their patients' age group and sex were similar to those of our study. Nearly 39% of them had comorbidities such as HT, DM, CHD, and COPD. Almost 35% of them had Stage 4 disease. These disease features led to better outcomes. Eight (28.6%) patients died.[8]

The most common symptoms that led to hospital presentation were dyspnea, dry cough, fever, and fatigue. Ground-glass consolidation or patchy appearance with peribronchial thickening resembling bronchopneumonia, typical for COVID-19, was observed in HRCT in 29 (67.4%) patients [samples, [Figure 1], [Figure 2], [Figure 3], [Figure 4]. There were no HRCT findings in 14 (33.6%) patients; their diagnosis was made by PCR analysis. Zhang et al. reported similar symptom percentage to our study.[8] Deng et al. reported 78 positive patients with COVID-19 symptoms by performing RT-PCR and HRCT. Fourteen (17.95%) patients had positive RT-PCR test. There were 37 (47.44%) patients with a positive computed tomography scan as typical for COVID-19. These results were also similar to those of our study.

Anemia was observed in seven (16.2%) patients (<Hb 10 g/dL) in the present study. Two patients had severe neutropenia (<100/ml) with fever. One patient had severe thrombocytopenia (<10 × 103/ml) with no bleeding. Erythrocyte sedimentation rate (ESR), CRP, and LDH levels were high. Only five patients had low albumin levels. D-dimer level had elevated in 22 (51.1%) patients. Patients in the ICU had lower albumin and higher leukocyte count, CRP, CK-MB, troponin, LDH, and ferritin than the others and were statistically significant. Other laboratory findings were similar to those of other patients. In a recent meta-analysis of 19 articles about COVID-19 in the normal population, Rodriguez et al. reported decreased albumin levels (75.8%), high CRP (58.3%), high LDH (57%), and high ESR.[12] In their study, Zhang et al. observed anemia (75%), leukopenia (32.1%), and low albumin levels. High levels of LDH and CRP were found. D-dimer had elevated in 11 (39%) patients.[8] There were small differences to our study laboratory findings. Low albumin levels predicted worse nutritional status. Worse nutritional status was related with cancer mortality. Moreover, high CRP levels were associated with an increased risk of ICU and 30-day mortality.[13]

Cancer diagnosis had a higher risk of acquiring severe events. However, cancer patients received the same treatments as normal population with COVID 19.[10] We used a broad-spectrum antibacterial therapy for empirical purpose. All patients received a low-molecular-weight heparin for thromboprophylaxis. Chloroquine, a common antimalarial and anti-rheumatism drug, was used. Antiviral agents including oseltamivir, favipiravir, and azithromycin which is also a macrolide antibacterial were used solely or in combination with chloroquine or other antiviral agents. An immune plasma exchange was done in one patient. All procedures were followed according to the guidelines.[11],[14],[15] Zhang et al. reported that 71.4% of their patients received antiviral agents. They also used systemic steroids which could cause opportunistic infections, especially in the ICU patients.[8]

In our cohort, admission to ICU, receiving mechanical ventilation support, and death were accepted as severe events. In 21 (48.8%) patients, severe events developed and were hospitalized in the ICU. Seventeen (39.5%) of them needed invasive mechanical ventilation. Others needed nasal oxygen and noninvasive mechanical ventilation. Only one patient recovered and was discharged. Twenty patients died (46.5%). Majority of them died due to ARDS and septic shock (85%). The median survival was 13 days and 10-day survival rate was 65.5%. Presence of heart disease including congestive heart disease, coronary artery disease, and atrial fibrillation; previous surgeries to the respiratory system (lobectomy); and presence of dyspnea at admission were significantly associated with death. In addition, invasive mechanical ventilation and intubation were linked to less survival outcomes. Use of ARBs was slightly related to a better survival outcome and contrarily presence of suspicious initial HRCT findings for COVID-19 was slightly related to worse outcome, those of which were not statistically significant. Zhang et al. showed that 53.6% of their cancer patients developed severe events and 8 (28.6%) patients died. Five of them died due to ARDS.[8] In our study, the mortality percentage was higher than that of similar studies in literature. We believed that majority of our cancer patients had Stage 3 or 4 diseases and all of them had comorbidities which could cause COVID-19 infection to settle more easily. Moreover, most of our patients had lung involvement, which was typical for COVID-19.

Our findings supported the fact that cancer patients were more affected by COVID-19 disease than the normal population. It was not appropriate to generalize because our study was retrospective and single centered and did not compare the findings with noncancer patients with COVID-19 disease. Furthermore, the results cannot be applied to other countries with different cancer epidemiology and practice.

Ethical approval

The Ethics Committee of Gulhane Training and Research Hospital approved the study with 172 ethical committee number on May 14, 2020. All procedures were carried out according to the Helsinki declaration of 1975 (revised in 2008), and all procedures adhered to the ethical standards of the responsible committee on human experimentation (institutional and national).

Acknowledgments

We thank the Management of the Gulhane Training and Research Hospital and the Health Ministry of Turkey.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Li Q, Guan X, Wu P, Wang X, Zhou L, Tong Y, et al. Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia. N Engl J Med 2020;382:1199-207.  Back to cited text no. 1
    
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Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet 2020;395:1054-62.  Back to cited text no. 4
    
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Wu Z, McGoogan JM. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: Summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention. JAMA 2020;323:1239-42.  Back to cited text no. 5
    
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Liang W, Guan W, Chen R, Wang W, Li J, Xu K, et al. Cancer patients in SARS-CoV-2 infection: A nationwide analysis in China. Lancet Oncol 2020;21:335-7.  Back to cited text no. 6
    
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Grein J, Ohmagari N, Shin D, Diaz G, Asperges E, Castagna A, et al. Compassionate use of remdesivir for patients with severe Covid-19. N Engl J Med 2020;382:2327-36.  Back to cited text no. 11
    
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Rodriguez-Morales AJ, Cardona-Ospina JA, Gutiérrez-Ocampo E, Villamizar-Peña R, Holguin-Rivera Y, Escalera-Antezana JP, et al. Clinical, laboratory and imaging features of COVID-19: A systematic review and meta-analysis. Travel Med Infect Dis 2020;34:101623.  Back to cited text no. 12
    
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Koozi H, Lengquist M, Frigyesi A. C-reactive protein as a prognostic factor in intensive care admissions for sepsis: A Swedish multicenter study. J Crit Care 2020;56:73-9.  Back to cited text no. 13
    
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Cao B, Wang Y, Wen D, Liu W, Wang J, Fan G, et al. A trial of lopinavir-ritonavir in adults hospitalized with severe COVID-19. N Engl J Med 2020;382:1787-99.  Back to cited text no. 14
    
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Chen Z, Hu J, Zhang Z, Jiang S, Han S, Yan D, et al. Efficacy of hydroxychloroquine in patients with COVID-19: Results of a randomized clinical trial. MedRxiv 2020. Doi: 10.1101/2020.03.22.20040758.  Back to cited text no. 15
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

 
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    -  Yilmaz G
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