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D-Dimer As a Prognostic Indicator in Critically Ill Patients Hospitalized with COVID-19 in Leishenshan Hospital, Wuhan, China

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D-Dimer As a Prognostic Indicator in Critically Ill Patients Hospitalized with COVID-19 in Leishenshan Hospital, Wuhan, China ORIGINAL RESEARCH published: 21 December 2020 doi: 10.3389/fphar.2020.600592 D-Dimer as a Prognostic Indicator in Critically Ill Patients Hospitalized With COVID-19 in Leishenshan Hospital, Wuhan, China Jinpeng Li 1†, Zeming Liu 2†, Gaosong Wu 1†, Meilin Yi 3†, Yongfeng Chen 4†, Kun Li 5, Xiaoming Xu 6, Linqi Xiao 7, Qian Wu 8*, Jincao Chen 8* and Xiaohui Wu 8* 1Department of Thyroid and Breast Surgery, Zhongnan Hospital of Wuhan University, Wuhan, China, 2Department of Plastic Surgery, Zhongnan Hospital of Wuhan University, Wuhan, China, 3Department of Burn and Plastic Surgery, College of Traditional Chinese Medicine, Three Gorges University and Yichang Hospital of Traditional Chinese Medicine, Yichang, China, 4Medical 5 Edited by: Department, Zhongnan Hospital of Wuhan University, Wuhan, China, Department of Hepatobiliary and Pancreatic Surgery, Zhongnan Hospital of Wuhan University, Wuhan, China, 6Department of Medical Records and Statistics, The Central Hospital of Annalisa Capuano, Wuhan, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China, 7Hospital Management University of Campania Luigi Vanvitelli, Institute, Zhongnan Hospital of Wuhan University, Wuhan, China, 8Department of Neurosurgery, Zhongnan Hospital of Wuhan Italy University, Wuhan, China Reviewed by: Annalisa Ruggeri, Laboratori di Ricerca, Bambino Gesù Background: D-dimer is a small protein fragment and high levels of D-dimer have been Ospedale Pediatrico, Italy associated with increased mortality in patients presenting to emergency departments with Klara Komici, University of Molise, Italy infection. Previous studies have reported increased levels of D-dimer in COVID-19; *Correspondence: however, it is unclear whether an increased D-dimer level provides early warning of Xiaohui Wu poor prognosis. Therefore, this study aimed to assess the usefulness of D-dimer as an [email protected] early indicator of prognosis in patients with coronavirus disease (COVID-19). Jincao Chen [email protected] Methods: We conducted a retrospective study of patients with COVID-19 admitted to Qian Wu [email protected] Leishenshan Hospital in Wuhan, China, from February 15 to March 30, 2020. The final date †These authors have contributed of follow-up was April 11, 2020. equally as Senior Authors Results: Of the 1,643 patients with COVID-19, 691 had elevated D-dimer levels. Their Specialty section: median age was 65 years. Of the patients with elevated D-dimer levels, 45% had This article was submitted to comorbidities, with cardiovascular disease (205 [29.7%]) being the most common. Cardiovascular and Smooth fl Muscle Pharmacology, Patients with elevated D-dimer were more likely to require treatment with high- ow a section of the journal oxygen, anticoagulation, antibiotics, and admission to the intensive care unit They Frontiers in Pharmacology were also more likely to have increased interleukin-6, monocytes, and lymphocytes. Received: 30 August 2020 Patients with elevated D-dimer levels had significantly higher mortality than those with Accepted: 23 November 2020 Published: 21 December 2020 normal or low D-dimer levels. Citation: Conclusion: In patients with COVID-19, elevated D-dimer was associated with abnormal Li J, Liu Z, Wu G, Yi M, Chen Y, Li K, Xu X, Xiao L, Wu Q, Chen J and Wu X immunity, underlying disease, increased disease severity, and increased mortality. Taken (2020) D-Dimer as a Prognostic together, D-dimer may be a marker for the early warning of disease severity and increased Indicator in Critically Ill Patients fi Hospitalized With COVID-19 in risk of death. These ndings provide insights into the potential risk of elevated D-dimer in Leishenshan Hospital, Wuhan, China. patients with COVID-19. Front. Pharmacol. 11:600592. doi: 10.3389/fphar.2020.600592 Keywords: SARS–CoV–2, prognostic indicator, critically ill patients, COVID-19, d-dimer Frontiers in Pharmacology | www.frontiersin.org 1 December 2020 | Volume 11 | Article 600592 Li et al. D-Dimer Indicated for COVID-19 INTRODUCTION METHODS A cluster of acute respiratory illness subsequently recognized as Study Design and Participants coronavirus disease (COVID-19), occurred in Wuhan, China, in This retrospective review of medical records included December 2019, (Epidemiology Working Group for NCIP 1643 COVID-19 patients admitted to Leishenshan Hospital Epidemic Response, Chinese Center for Disease Control and in Wuhan, China, from February 15 to March 30, 2020. The Prevention, 2020; Hui et al., 2020) and it subsequently spread final date of follow-up was April 11, 2020. All patients were to all regions of the world. Between December 2019 and April 27, diagnosed with COVID-19 according to the World Health 2020, almost three million people were diagnosed with COVID- Organization interim guidance and the COVID-19 19 worldwide. In addition to Wuhan in China, Korea, Italy, the Prevention and Control guidelines (seventh edition) United States, France, Germany, Iran, and the United Kingdom published by the National Health Commission of China. The have experienced major national epidemics (Huang et al., 2020). patients provided oral consent. This study was approved by the Common symptoms of COVID-19 include fever, dyspnea, dry Research Ethics Committee of Wuhan University Zhongnan cough, fatigue, and myalgia. Common laboratory findings include Hospital (approval number 2020004). normal or decreased leukocyte counts, lymphopenia, and increased C-reactive protein, and radiography usually shows Data Collection evidence of pneumonia (Huang et al., 2020). Wand et al. We reviewed the clinical and laboratory findings, demographic reported that among 138 hospitalized patients with COVID-19 data, treatment, and chest computed tomography (CT) scans of pneumonia, 26% require intensive care unit (ICU) care, and the all 1643 COVID patients admitted to Leishenshan Hospital mortality is 4.3% (Wang et al., 2020). during the study period. All data were collected from electronic In the patients with COVID-19 pneumonia, the mortality rate medical records using a customized data collection form. Two increases with age. Older people are more likely to have physicians at Leishenshan Hospital collected and analyzed all comorbidities such as diabetes mellitus, hypertension, cardiac data. All the laboratory outcomes were measured in the first disease, and cancer. A recent study reported that older age was time on admission. The methods for laboratory diagnosis of associated with greater risk of development of acute respiratory COVID-19 were the same as those reported previously (Huang distress syndrome and death, which was probably due to lower et al., 2020). In brief, throat swab samples were collected from levels of immunity in general (Ciceri et al., 2020; Wu et al., 2020). patients with suspected COVID-19 pneumonia and Additionally, hypertension was reported to be the most common immediately tested for severe acute respiratory syndrome comorbidity in an analysis of fatal cases of COVID-19 pneumonia, coronavirus 2 (SARS-CoV-2) RNA. All patients had at least followed by diabetes and coronary heart disease (Varga et al., 2020; three throat swab samples collected. The RT-PCR assay for the Zhou et al., 2020). A higher D-dimer level (>1 μg/ml) appeared to detection of SARS-CoV-2 nucleic acid was performed be associated with an increased risk of death. according to the manufacturer’sprotocol(BioGerm, D-dimer is a fibrin degradation product, a small protein Shanghai Berger Medical Technology Company, Pudong fragment that is released into the blood when a blood clot is New District, China). Venous blood samples were collected degraded by fibrinolysis (Adam et al., 2009). A diagnosis of from the antecubital fossa and tested for immunoglobulin G thrombosis can be made by determining the D-dimer (IgG) and immunoglobulin M (IgM) antibodies to SARS- concentration: the D-dimer level is increased when the CoV-2. coagulation system is activated by thrombosis or disseminated intravascular coagulation. A high level of D-dimer may also be a Statistical Analysis sign of deep venous thrombosis, pulmonary embolism, or Continuous variables with a normal distribution were reported as disseminated intravascular coagulation (DIC) (Ranasinghe and the mean ± standard deviation; otherwise, they were reported as Bonser, 2010). Zhou et al. reported that a high level of D-dimer the median and interquartile range (IQR). Categorical variables may help in the early clinical diagnosis of COVID-19 (Zhou et al., were described as frequencies and percentages. Two-sample 2020). Furthermore, in the 2003 severe acute respiratory t-tests or Mann-Whitney tests were used to test whether there syndrome (SARS) epidemic, most patients had were any significant differences in the mean of continuous thrombocytopenia and elevated levels of D-dimer (Tan et al., variables between the higher and lower D-dimer groups. The 2005). Similarly, elevated D-dimer levels have also been reported proportions of categorical variables in these two groups were in patients with Ebola (Smither et al., 2019). Although there have compared using the chi-square test or Fisher’s exact test when the been some reports on increased levels of D-dimer in COVID-19 cell size was small. Univariate and multivariate logistic regression patients, it is unclear whether an increased D-dimer level is an analyses were performed to determine the relationship between early warning of a poor prognosis. D-Dimer level and the prognosis of COVID-19 patients. Patient In this study we analyzed the D-dimer
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