key: cord-0933695-7uivwv53 authors: Zhang, Zhu; Xi, Linfeng; Zhang, Shuai; Zhang, Yunxia; Pang, Wenyi; Wang, Yimin; Li, Chenghong; Zhai, Zhenguo; Wang, Chen title: Awareness and Prophylaxis of Venous Thromboembolism in Patients with COVID-19: A National Cross-Sectional Survey in Epidemic Era date: 2020-10-01 journal: J Atheroscler Thromb DOI: 10.5551/jat.58933 sha: 97201885611688a474bcde3d0f7e250899393ca0 doc_id: 933695 cord_uid: 7uivwv53 Aim: Patients with acute infectious diseases are at an increased risk of venous thromboembolism (VTE). Clinicians should be aware of the VTE risk in patients with COVID-19, many of whom present with severe coagulation disorders. Method: We used an online platform to conduct a cross-sectional questionnaire survey among doctors in mainland China in March 2020. The questionnaire was designed to figure out the clinician's current awareness of VTE prevention and detection rates, as well as the current status of VTE prophylaxis in patients with COVID-19. Results: We collected 1,636 replies, of which 1,579 were valid. Among these, 991 (63%) clinicians were involved directly in frontline treatment. Most of the clinicians (1,492, or 94%) thought it was necessary to assess the VTE risk in patients with COVID-19. However, only 234 (24%) clinicians performed appropriate assessment during the COVID-19 outbreak. For patients with mild/moderate COVID-19, 752 (76%) clinicians would prescribe exercise and water to prevent VTE. For patients with severe COVID-19, 448 (45%) clinicians would prescribe mechanical devices if the patient had a high bleeding risk, and 648 (65%) clinicians would choose LMWH as prophylaxis if the patient had a low bleeding risk. The VTE detection rate was not that high in both mild/moderate and severe patients. Conclusion: Although most clinicians recommended prescribing VTE prophylaxis to patients with COVID-19, the practice still needs to be improved. A real-world registry to investigate the true incidence of VTE, and the effect of prescribing appropriate prophylaxis for patients with COVID-19, is necessary in the future. adapted prophylaxis for the patients will reduce the incidence and mortality of hospital-associated VTE, which may also contribute to reduced mortality in patients with COVID-19. On February 9, 2020, the China Pulmonary Thromboembolism Registry Study (CURES) network issued the "Prevention and Treatment of Venous Thromboembolism Associated with Coronavirus Disease 2019 Infection: A Consensus Statement before Guidelines" (hereafter referred to as the "Statement") 9) . The "Statement," attached in Supplementary Table 1 , recommended to screen all patients with COVID-19 for VTE risk and prescribe appropriate prevention strategies for them. However, the current clinical practice is still uncertain, and the VTE detection rate in patients with COVID-19 remains unknown. Therefore, in this study, we designed a survey to understand clinicians' current of the VTE risks among patients with COVID-19, the status of prophylaxis, and the estimated VTE detection rate. In March 2020, a cross-sectional questionnaire survey was designed for online use by the CURES network. Supplementary Table 2 presents the English version. The survey was distributed to clinicians through the Tencent online platform (supported by the Tencent Customer Research and User Experience Design Center) between March 13-17, 2020, in mainland China. It was divided into three parts. The first part recorded the baseline information of the physicians, including the following nine demographic variables: gender, age, department, job title, level of the hospital, location of the licensed hospital, present location, whether they had made VTE diagnosis and treatment and whether they were involved in treating patients with COVID-19. The second part consisted of seven questions that focused on the participant's risk assessment awareness and their backing of the "Statement." The third part consisted of 17 questions regarding the risk assessment, prophylaxis strategies, and VTE diagnosis in patients with COVID-19, specifically targeting doctors involved in treating patients with COVID-19. All participants provided informed consent, and the Ethics Committee of the China-Japan Friendship Hospital approved the study. We analyzed the survey data with descriptive sta- From December 2019, a series of unexplained pneumonia cases occurred in the city of Wuhan, Hubei Province, China 1) . On February 11, 2020, the World Health Organization (WHO) officially named the disease Coronavirus Disease 2019 . Since December 2019, millions of people have been infected with COVID-19; hundreds of thousands have died from virus-related complications. COVID-19 has become a global crisis. According to reports from frontline doctors treating patients with COVID-19, nearly 20% of the recorded patients have presented with coagulation disorders, and almost all the patients who were severely affected suffered from coagulation dysfunctions. The pathological findings support that microthrombosis can occur in most organs of the patients infected with COVID-19 2, 3) . A prospective study from Germany performed autopsies on 12 patients who died of COVID-19. They found that the incidence rate of deep venous thrombosis was 58%, and pulmonary embolism (PE) was the direct cause of death in four patients 4) . As an acute systematic infectious disease, COVID-19 is a significant risk factor for venous thromboembolism (VTE) 5) . The risk of VTE further increases when the patient is experiencing complications due to immobilization, an active malignancy, or obesity, especially in elderly patients or those with an underlying disease 6) . Some studies have associated VTE and COVID-19 7) , which should not be considered a random event. VTE is a fatal disease, and 55-60% of the cases are directly related to hospitalization 8) . However, it is preventable and treatable if identified early. Risk-result, 1,579 valid survey results used in the analysis, among which 991 (63%) were involved directly in the frontline treatment of patients with COVID-19 ( Table 1) . Most of the participants (83%) aged between 31-60 years. Of these participants, 51% were women, and 49% were men. Besides, 45% of participants were attending, or deputy chiefs and 61% of the participants were pulmonary and critical care medical doctors. Many doctors around the country signed up to assist in the Hubei province, which was the major COVID-19 hotspot in China, to support the frontline healthcare effort. Most clinicians worked in tertiary or teaching hospitals (79%). Fig. 1 shows the distribution of participants, most of whom were from the provinces of Hubei (557), Shanxi (153), and Henan (106); 92% of the participants claimed that they had previous experience with the diagnosis and treatment of VTE. tistics. Categorical data were presented as N (%), and continuous data were presented as means (with standard deviation, SD) or medians (with range). Additional subgroup analyses were performed between the physicians who were directly involved in treating patients with COVID-19 and those who were not. Frontline doctors were then further divided into two groups based on whether they worked in the Hubei Province or not. Fisher's exact test was used to compare quantitative data between subgroups. A P-value 0.05 was considered statistically significant. All statistical analysis was performed using the SPSS 26.0 software (IBM). The 1,636 clinicians participated in this questionnaire, among which 55 did not complete the questions and 2 filled in the forms incorrectly. As a (79%). However, the participants who were involved in treating patients with COVID-19 prioritized these factors differently. Frontline clinicians paid more attention to the risk factor of underlying diseases compared with non-frontline clinicians (frontline vs. nonfrontline: 90% vs. 85%, P 0.01) ( Table 3) . However, most non-frontline clinicians considered inserting a central venous catheter to be the most significant risk factor for VTE in patients with COVID-19 (frontline vs. non-frontline: 77% vs. 83%, P 0.01) ( Table 3) . Among the frontline doctors, those enlisted outside Hubei Province linked more importance to risk factors such as dehydration and hypotension Of the 991 participating frontline workers, 23% treated more than 50 patients with COVID-19. Most of them were in Hubei Province (Hubei vs. outside Hubei: 36% vs. 4%, P 0.01) ( Table 2) . Regardless of whether they worked on the frontline or not, the vast majority of the participants (1492, or 94%) believed that patients with COVID-19 have an increased risk of suffering from VTE and VTE risk assessment is essential. The top five VTE risk factors that the participants selected were immobilization (95%), advanced age (92%), underlying diseases (88%), concurrent infection (88%), and central venous catheterization the "Statement." The rate of correctly performed VTE risk assessment was significantly different between Hubei province and the rest of mainland China (9% vs. 15%, respectively, P 0.05). Regarding the choice of treatment to prevent VTE in mild/moderate patients with COVID-19 with a low VTE risk, 76% of the clinicians would choose to prescribe exercise and water. (Hubei vs. outside Hubei: 74% vs. 79%, P 0.04). 69% of the clinicians would prescribe low-molecular-weight heparin (LMWH) for VTE prophylaxis in mild patients with COVID-19 who have a high VTE risk (Hubei vs. outside Hubei: 72% vs. 65%, P 0.01). Table 4 shows these results. For severely/critically ill patients with COVID-19 who have a low bleeding risk, 65% of the clinicians (Hubei vs. outside Hubei: 67% vs. 78%, P 0.01; 63% vs. 71%, P 0.01) (Supplementary Table 3 ). We also found that compared with residents, senior doctors had a more thorough understanding of the VTE risk factors related to COVID-19, including the effects of dehydration, hypotension or shock, and mechanical ventilation (residents vs. attendings or deputy chiefs: 58% vs. 77%, P 0.01; 55% vs. 69%, P 0.01; 53% vs. 64%, P 0.01), while there was little difference among different levels of hospitals for VTE awareness (Supplementary Table 4) . During our survey, we only asked the frontline workers (n 991) about implementing the VTE risk assessment. The results showed that a considerable proportion of the surveyed clinicians (76%) did not conduct the VTE risk assessment or completely follow charged from the hospital, 94% of the clinicians (Hubei vs. outside Hubei: 93% vs. 95%, P 0.275) claimed that they would assess the risk of VTE in the patient and take the appropriate preventive measures, which is consistent with the "Statement." If the clinicians believed that a discharged patient had a risk for VTE, 45% would choose to tell the patient to exercise/drink water, 35% would choose to prescribe rivaroxaban (Hubei vs. outside Hubei: 34% vs. 37%, P 0.46) and 7% would choose to use LMWH (Hubei vs. outside Hubei: 9% vs. 5%, P 0.04) (Supplementary Fig. 1) . We asked the frontline clinicians about their choice of diagnostic methods for patients with COVID-19 suspected of having VTE. The top five preferred diagnostic methods were D-dimer (93%), compression ultrasonography (CUS) (87%), arterial blood gas (ABG) (65%), computed tomography pulmonary angiography (CTPA) (63%) and echocardiography (58%). No significant difference was observed between the clinicians working in Hubei Province and their peers in other provinces (Fig. 2) . The survey included the detection rate of VTE in patients with COVID-19 handled by frontline doctors. We found that the detection rate of VTE was low in patients with COVID-19. Among patients with mild/moderate COVID-19, most clinicians (n 637, 68%) reported that they had never diagnosed a VTE event (Hubei vs. outside Hubei: 61% vs. 79%, P 0.05), while the vast majority (n 871, 93%) believed would choose LMWH as prophylaxis. Fewer than half (45%) of the clinicians would choose mechanical devices for patients with high bleeding risk, 20% would still choose LMWH, while 11% would select exercise/drinking water as a treatment for patients with a high bleeding risk and severe COVID-19 symptoms. For the participants who worked in Hubei Province, only 37% would choose mechanical devices, 26% would choose LMWH, and 12% would choose exercise/drinking water as a treatment for patients with COVID-19 who had severe symptoms and high bleeding risk (Table 4) . For severe/critically ill patients with low bleeding risk, the residents were more likely to prescribe unfractionated heparin (UFH), compared with senior doctors (residents vs. attendings or deputy chiefs: 9% vs. 4%, P 0.02) (Supplementary Table 5 ). Doctors in tertiary hospitals tended to prescribe LMWH, compared with those in primary or secondary hospitals (tertiary or teaching hospitals vs. primary or secondary hospitals: 30% vs. 57%, P 0.01) (Supplementary Table 6 ). For severe/critically ill patients who have a high bleeding risk (Supplementary Table 7) , senior doctors were more likely to choose mechanical prevention instead of prescribing LMWH (residents vs. attendings or deputy chiefs: 34% vs. 48%, P 0.01) (Supplementary Table 5 ). There was no significant difference among different hospital levels (Supplementary Table 6 ). After a COVID-19 patient is cured and dis- The figure shows that the top five diagnostic methods are: D-dimer testing (93%), venous ultrasound of lower extremities (87%), arterial blood gas analysis (65%), CT pulmonary angiography (63%) and Echocardiography (58%). There is no significant difference between the results in Hubei Province and outside of it, which are both consistent with the overall trend. practice. Also, senior doctors or doctors working in tertiary or teaching hospitals were more likely to comply with the "Statement" and chose reasonable VTE prophylaxis. In other words, clinical experience and standard education have profound impacts on the selection of VTE prophylaxis. Intensive training will be needed to solve this problem in the future. Another interesting finding from our survey was that frontline clinicians felt that underlying diseases represented the most concerning VTE risk factor, as opposed to the clinicians who were not involved in treating patients with COVID-19, who were mostly concerned about the central venous catheter. The reason for this may be that frontline doctors are treating many hospitalized patients with COVID-19, who are severely ill and mostly suffer from underlying diseases. Coagulopathy is known to have occurred in the majority of patients who died of COVID-19. Multiple mechanisms are involved in this process, including endothelins and inflammatory biomarkers 12) . The SARS-Cov-2 virus binds to the host cells via the Angiotensin-Converting Enzyme 2 Receptor (ACE2R), which is universal in all major organs, especially the lungs, heart, veins, and arteries. ACE2Rs are expressed widely in endothelial cells, which can explain their susceptibility to thromboembolic events 12) . On the other hand, Inflammation may also increase thrombosis risk. Inflammation markers are elevated significantly in patients with COVID-19, which are related to poor prognosis. SARS-Cov-2 activates the inflammatory cells, such as macrophages. As inflammation worsens, the release of pro-inflammatory cytokines progresses into a cytokine storm, causing acute respiratory distress syndrome (ARDS) and disseminated intravascular coagulation (DIC) 13) . A histological examination of patients with COVID-19 showed prominent endotheliitis and accumulated inflammatory cells 14) . Endothelial cell infection and immune-mediated endotheliitis both play an important role in COVID-19 related coagulopathy. Coagulation dysfunction may occur in severe cases of both COVID-19 and VTE. Recent studies have shown that severe COVID-19 cases often have major coagulation abnormalities, as the level of D-dimer is increased and significantly higher than that of mild/moderate patients. The level of fibrin degradation products (FDP) is also significantly increased. These levels are closely related to the mortality in patients with COVID-19 [15] [16] [17] . Besides, D-dimer is of great significance in the diagnosis and treatment guidelines of VTE. It has a high sensitivity in acute PE diagnosis (92-100%), and a high negative predictive value as well. Recent emerging evidence implies that D-dimer is also valuable for COVID-19 that the VTE incidence was lower than 5% (Hubei vs. outside Hubei: 91% vs. 96%, P 0.01). Similarly, more than half of the surveyed clinicians (n 433, 51%) claimed that VTE did not occur when they provided healthcare to severely/critically ill patients with COVID-19 (Hubei vs. outside Hubei: 40% vs. 70%, P 0.05). During the pandemic, the VTE detection rate in severe/critically ill patients with COVID-19 in Hubei was generally higher than that of outside Hubei (Hubei vs. outside Hubei: 60% vs. 30%, P 0.05). Among all the participants in this survey (n 1,579), the majority of the involved clinicians (n 1,537, 97%) believed that the "Statement" had clinical significance and could serve as a reference for clinical practice. Still, only 64% of them said they had read the "Statement" (either the full text or its interpretation). However, the number of frontline clinicians who had read the "Statement" was higher than that of non-frontline clinicians (frontline vs. nonfrontline: 72% vs. 51%, P 0.05). This study is the first survey to focus on VTE prophylaxis in patients with COVID-19 in mainland China. It shows the inadequate VTE prophylaxis during the COVID-19 pandemic and the existing gap between clinical work and evidence-based medicine. Most clinicians believe that patients with COVID-19 are at risk of VTE, and evaluating VTE risks is valuable for these patients. However, this was inconsistent with the real-world scenario, which showed a low VTE assessment and implementation rate of current VTE prevention measures, leading to a low VTE detection rate. Over the past 10 years, Chinese clinicians' ability to diagnose and treat VTE has improved with the support of CURES. From 1997 to 2008, the hospitalassociated VTE mortality rate decreased from 25.1% to 8.7% 10) . At the same time, the awareness of VTE among Chinese clinicians has increased 11) . The results of our study showed that Chinese clinicians demonstrate high awareness of VTE and generally believe that patients with COVID-19 are at risk of VTE. Meanwhile, it showed that there is little difference in VTE awareness among hospitals of different levels. This may indicate that our previous work can well promote the standardization of VTE diagnosis and treatment in China. However, our findings showed that most of the clinicians did not actually assess the VTE risk in patients with COVID-19, and the prophylaxis was not appropriately implemented, especially for the severe COVID-19 cases; this is partially due to the gap between the guidelines and clinical was conducted through an online questionnaire, which may include the risk of response bias, thus having inaccurate and one-sided collected data. Finally, the sample size of this study is small and cannot represent the overall population. Through this online survey, we have found that most clinicians are generally aware of VTE prophylaxis for patients with COVID-19 and that the clinical practice still needs to be improved. However, the diagnosis of VTE may still be missed due to the unspecific clinical characteristics of VTE and difficulty in using CTPA as a result of the highly contagious features of COVID-19. VTE risk assessment and prophylaxis measurements, especially in severe COVID-19 cases, should be taken as early as possible. Additionally, we should also look for other simple and feasible methods to assist in the diagnosis of VTE, which will contribute to reducing the mortality of COVID-19. A realworld registry study is needed to investigate the true incidence of VTE and the effect of appropriate prophylaxis for patients with COVID-19. Author contributions: Zhenguo Zhai had full access to all the data in the study and takes responsibility for the content of the manuscript. Zhu Zhang and Shuai Zhang conceived and designed the study. Zhu Zhang and Linfeng Xi integrated data and take responsibility for the accuracy of the data analysis. Linfeng Xi and Zhu Zhang analyzed the data and wrote the manuscript. Yunxia Zhang, Wenyi Pang, Yimin Wang, Chenghong Li and Chen Wang contributed to the interpretation of the data and clinical inputs. All authors were involved in the revision of the manuscript for important intellectual content and approved the final version to be published. The authors would like to express their gratitude to Edit-Springs (https://www.editsprings.com/) for the expert linguistic services provided. prognosis and risk stratification. According to the International Society of Thrombosis and Haemostasis (ISTH), a markedly increased D-dimer level is associated with high mortality in patients with COVID-19. When coagulation dysfunction occurs in patients with COVID-19 18) , it is unclear whether the elevation of D-dimer indicates VTE development. Therefore, clinicians may overlook the abnormality of D-dimer levels, resulting in a decreased detection rate of VTE. With the continually improved understanding of COVID-19 related VTE, emerging evidence suggests that all hospitalized patients with COVID-19 (including non-critically ill patients) should receive prophylactic dose LMWH, unless they have contraindications (active bleeding and platelet count 25x10 9 per liter) 19) . A case report showed that a patient with COVID-19 who was not admitted to hospital because of mild symptoms developed PE 20) . It seems that the hypercoagulable state may exist for a long time in the course of COVID-19. Venous thrombotic events can occur in both mild and severe COVID-19 cases, who should receive anticoagulant therapy. However, in our study, a substantial number of clinicians would prescribe exercise and water to prevent VTE in mild/ moderate COVID-19 cases, which may not be enough for the prophylaxis. Our results showed that the promotion of the "Statement" is still insufficient. Although almost all clinicians could recognize its necessity and clinical significance, only 64% of them said they had previously read it, and the percentage of non-frontline clinicians was even lower. When faced with suspected VTE patients, clinicians who had not read the "Statement" might rely on their previous potentially inappropriate clinical experience to choose diagnostic measures, which can decrease the prevention and detection rates of VTE. During the pandemic, there are limitations on the various diagnostic measures for various reasons. Therefore, future research should consider new biomarkers to help clinicians in the decision-making process regarding the appropriate diagnosis and treatment for VTE apart from CTPA during the pandemic. For example, it may be necessary to closely monitor the changes in the D-dimer level, which is now addressed in the ISTH guidance. A recent study showed that dynamic changes in the D-dimer level are positively correlated with the severity and prognosis of COVID-19 21, 22) . This study has certain limitations. First of all, this study is an observational cross-sectional study, and further research is needed to verify whether the changes in the D-dimer levels can assist in identifying VTE in patients with COVID-19. Also, this study 4. In severe or critically ill COVID-19 patients at high risk of bleeding or with active bleeding contra-indicating temporarily pharmacological thromboprophylaxis, it is recommended to use IPC for VTE prevention 5. Pharmacological prevention with LMWH is recommended as first-line treatment in patients at low or moderate risk of bleeding and with no contraindication to antithrombotic drugs. In patients with severe renal impairment (creatinine clearance rate: <30 ml/min) it is recommended to use unfractionated heparin (UFH). 6. Mild and moderate COVID-19 patients isolated for medical treatment, especially those with fever and/or gastrointestinal symptoms (diarrhea and anorexia) should be rehydrated without delay. 7. Mild and moderate COVID-19 patients presenting acute medical diseases and assessed to have a high or moderate risk of VTE (PADUA or IMPROVE RAM), pharmacological prevention should be prescribed and LMWH is recommended as first-line treatment, in absence of contraindication. 8. Mild and moderate COVID-19 patients requiring surgical procedure or presenting traumatic conditions and assessed to have a high or moderate risk of VTE (CAPRINI RAM), pharmacological prevention should be prescribed and LMWH is recommended as first-line treatment, in absence of contraindication. 9. Mild and moderate COVID-19 patients perceived to have a persistent risk of VTE at the time of discharge, a prolonged out-patient VTE prophylaxis care should be considered with LMWH over DOAC use, caution due to potential drug-drug-interactions and/or frequent comorbidities. 10. Suspected mild and moderate COVID-19 patients should avoid sedentariness, dehydration, and should be encouraged to remain active with regular mobilization (ankle pump movements) and drinking appropriate volume of water during their isolation at home. 11. In case of DVT or PE suspicion, diagnosis should be primarily based on careful bedside clinical examinations and then objectively confirmed by imaging explorations (venous echo-doppler ultrasound, echocardiography and CTPA with mandatory clinical and protective conditions. 12. In COVID-19 patients suspected for VTE, or relevant examinations fail to be conducted due to restricted conditions, starting a curative anticoagulant parenteral treatment with LMWH as first-line treatment is recommended in absence of contraindication. Dear colleagues, the beginning of 2020 witnessed the outbreak and rapid spread of COVID-19 across the country. In this silent war, VTE becomes a hidden killer. 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Preventing hospital associated venous thromboembolism Prevention Treatment of VTE Associated with COVID-19 Infection Consensus Statement Group, Prevention and Treatment of Venous Hepatic dysfunction (INR 1.5) • Severe renal insufficiency (GFR 30 ml·min 1 ·m 2 ) • Admitted to ICU/CCU • Central venous catheterization • Rheumatic diseases • Active cancer • Male GFR = Glomerular filtration rate • Abdominal surgery: preoperative anemia/complex surgery (combined surgery, difficult separation or more than one anastomosis) surgical site bleeding • Hepatectomy: primary hepatocellular carcinoma, low preoperative hemoglobin and platelet counts • Cardiac surgery: longer extracorporeal circulation time • Thoracic surgery: pneumonectomy or total extended lung resection • Craniotomy, spine surgery, spinal trauma, free flap reconstruction surgery Supplementary Fig. 1. The preventive strategies for COVID-19 patients who have VTE risk on discharge Most of the participants chose multi-activity/drinking water or rivaroxaban as the main strategies for outpatients to prevent VTE COVID-19 = Coronavirus disease LMWH = Lowmolecular-weight heparin No conflicts of interest are involved in this manuscript.