Thrombosis, Bleeding, and the Observational Effect of Early Therapeutic Anticoagulation on Survival in Critically Ill Patients With COVID-19

Hanny Al-Samkari, Shruti Gupta, Rebecca Karp Leaf, Wei Wang, Rachel P Rosovsky, Samantha K Brenner, Salim S Hayek, Hanna Berlin, Rajat Kapoor, Shahzad Shaefi, Michal L Melamed, Anne Sutherland, Jared Radbel, Adam Green, Brian T Garibaldi, Anand Srivastava, Amanda Leonberg-Yoo, Alexandre M Shehata, Jennifer E Flythe, Arash Rashidi, Nitender Goyal, Lili Chan, Kusum S Mathews, S Susan Hedayati, Rajany Dy, Stephanie M Toth-Manikowski, Jingjing Zhang, Mary Mallappallil, Roberta E Redfern, Amar D Bansal, Samuel A P Short, Mark G Vangel, Andrew J Admon, Matthew W Semler, Kenneth A Bauer, Miguel A Hernán, David E Leaf, STOP-COVID Investigators, Carl P Walther, Samaya J Anumudu, Justin Arunthamakun, Kathleen F Kopecky, Gregory P Milligan, Peter A McCullough, Thuy-Duyen Nguyen, Shahzad Shaefi, Megan L Krajewski, Sidharth Shankar, Ameeka Pannu, Juan D Valencia, Kenneth A Bauer, Sushrut S Waikar, Zoe A Kibbelaar, Ambarish M Athavale, Peter Hart, Shristi Upadhyay, Ishaan Vohra, Ajiboye Oyintayo, Adam Green, Jean-Sebastien Rachoin, Christa A Schorr, Lisa Shea, Daniel L Edmonston, Christopher L Mosher, Alexandre M Shehata, Zaza Cohen, Valerie Allusson, Gabriela Bambrick-Santoyo, Noor Ul Aain Bhatti, Bijal Mehta, Aquino Williams, Samantha K Brenner, Patricia Walters, Ronaldo C Go, Keith M Rose, Miguel A Hernán, Amy M Zhou, Ethan C Kim, Rebecca Lisk, Lili Chan, Kusum S Mathews, Steven G Coca, Deena R Altman, Aparna Saha, Howard Soh, Huei Hsun Wen, Sonali Bose, Emily A Leven, Jing G Wang, Gohar Mosoyan, Pattharawin Pattharanitima, Emily J Gallagher, Allon N Friedman, John Guirguis, Rajat Kapoor, Christopher Meshberger, Katherine J Kelly, Chirag R Parikh, Brian T Garibaldi, Celia P Corona-Villalobos, Yumeng Wen, Steven Menez, Rubab F Malik, Carmen Elena Cervantes, Samir C Gautam, Mary C Mallappallil, Jie Ouyang, Sabu John, Ernie Yap, Yohannes Melaku, Ibrahim Mohamed, Siddhartha Bajracharya, Isha Puri, Mariah Thaxton, Jyotsna Bhattacharya, John Wagner, Leon Boudourakis, H Bryant Nguyen, Afshin Ahoubim, Leslie F Thomas, Dheeraj Reddy Sirganagari, Pramod K Guru, Yan Zhou, Paul A Bergl, Jesus Rodriguez, Jatan A Shah, Mrigank S Gupta, Princy N Kumar, Deepa G Lazarous, Seble G Kassaye, Michal L Melamed, Tanya S Johns, Ryan Mocerino, Kalyan Prudhvi, Denzel Zhu, Rebecca V Levy, Yorg Azzi, Molly Fisher, Milagros Yunes, Kaltrina Sedaliu, Ladan Golestaneh, Maureen Brogan, Jyotsana Thakkar, Neelja Kumar, Michael J Ross, Michael Chang, Ritesh Raichoudhury, Akshay Athreya, Mohamed Farag, Edward J Schenck, Soo Jung Cho, Maria Plataki, Sergio L Alvarez-Mulett, Luis G Gomez-Escobar, Di Pan, Stefi Lee, Jamuna Krishnan, William Whalen, David Charytan, Ashley Macina, Anand Srivastava, Alexander S Leidner, Carlos Martinez, Jacqueline M Kruser, Richard G Wunderink, Alexander J Hodakowski, Juan Carlos Q Velez, Eboni G Price-Haywood, Luis A Matute-Trochez, Anna E Hasty, Muner M B Mohamed, Rupali S Avasare, David Zonies, David E Leaf, Shruti Gupta, Rebecca Karp Leaf, Rachel Rosovsky, Meghan E Sise, Erik T Newman, Samah Abu Omar, Kapil K Pokharel, Shreyak Sharma, Harkarandeep Singh, Simon Correa, Tanveer Shaukat, Omer Kamal, Wei Wang, Meghan Lee, Ian A Strohbehn, Jiahua Li, Ariel L Mueller, Roberta E Redfern, Nicholas S Cairl, Gabriel Naimy, Abeer Abu-Saif, Danyell Hall, Laura Bickley, Chris Rowan, Farah Madhani-Lovely, Vasil Peev, Jochen Reiser, John J Byun, Andrew Vissing, Esha M Kapania, Zoe Post, Nilam P Patel, Joy-Marie Hermes, Anne K Sutherland, Amee Patrawalla, Diana G Finkel, Barbara A Danek, Sowminya Arikapudi, Jeffrey M Paer, Peter Cangialosi, Mark Liotta, Jared Radbel, Sonika Puri, Jag Sunderram, Matthew T Scharf, Ayesha Ahmed, Ilya Berim, Jayanth S Vatson, George Karp, Shuchi Anand, Joseph E Levitt, Pablo Garcia, Suzanne M Boyle, Rui Song, Jingjing Zhang, Sang Hoon Woo, Xiaoying Deng, Goni Katz-Greenberg, Moh'd A Sharshir, Vadym V Rusnak, Muhammad Imran Ali, Anip Bansal, Amber S Podoll, Michel Chonchol, Sunita Sharma, Ellen L Burnham, Arash Rashidi, Rana Hejal, Eric Judd, Laura Latta, Ashita Tolwani, Timothy E Albertson, Jason Y Adams, Steven Y Chang, Rebecca M Beutler, Carl E Schulze, Etienne Macedo, Harin Rhee, Kathleen D Liu, Vasantha K Jotwani, Jay L Koyner, Chintan V Shah, Vishal Jaikaransingh, Stephanie M Toth-Manikowski, Min J Joo, James P Lash, Javier A Neyra, Nourhan Chaaban, Madona Elias, Yahya Ahmad, Rajany Dy, Alfredo Iardino, Elizabeth H Au, Jill H Sharma, Marie Anne Sosa, Sabrina Taldone, Gabriel Contreras, David De La Zerda, Hayley B Gershengorn, Alessia Fornoni, Salim S Hayek, Pennelope Blakely, Hanna Berlin, Tariq U Azam, Husam Shadid, Michael Pan, Patrick O'Hayer, Chelsea Meloche, Rafey Feroze, Kishan J Padalia, Jeff Leya, John P Donnelly, Andrew J Admon, Jennifer E Flythe, Matthew J Tugman, Emily H Chang, Brent R Brown, Amanda K Leonberg-Yoo, Ryan C Spiardi, Todd A Miano, Meaghan S Roche, Charles R Vasquez, Amar D Bansal, Natalie C Ernecoff, Sanjana Kapoor, Siddharth Verma, Huiwen Chen, Csaba P Kovesdy, Miklos Z Molnar, Ambreen Azhar, S Susan Hedayati, Mridula V Nadamuni, Shani Shastri, Duwayne L Willett, Samuel A P Short, Amanda D Renaghan, Kyle B Enfield, Pavan K Bhatraju, A Bilal Malik, Matthew W Semler, Anitha Vijayan, Christina Mariyam Joy, Tingting Li, Seth Goldberg, Patricia F Kao, Greg L Schumaker, Nitender Goyal, Anthony J Faugno, Greg L Schumaker, Caroline M Hsu, Asma Tariq, Leah Meyer, Ravi K Kshirsagar, Daniel E Weiner, Marta Christov, Jennifer Griffiths, Sanjeev Gupta, Aromma Kapoor, Savneek Chugh, Perry Wilson, Tanima Arora, Ugochukwu Ugwuowo, Hanny Al-Samkari, Shruti Gupta, Rebecca Karp Leaf, Wei Wang, Rachel P Rosovsky, Samantha K Brenner, Salim S Hayek, Hanna Berlin, Rajat Kapoor, Shahzad Shaefi, Michal L Melamed, Anne Sutherland, Jared Radbel, Adam Green, Brian T Garibaldi, Anand Srivastava, Amanda Leonberg-Yoo, Alexandre M Shehata, Jennifer E Flythe, Arash Rashidi, Nitender Goyal, Lili Chan, Kusum S Mathews, S Susan Hedayati, Rajany Dy, Stephanie M Toth-Manikowski, Jingjing Zhang, Mary Mallappallil, Roberta E Redfern, Amar D Bansal, Samuel A P Short, Mark G Vangel, Andrew J Admon, Matthew W Semler, Kenneth A Bauer, Miguel A Hernán, David E Leaf, STOP-COVID Investigators, Carl P Walther, Samaya J Anumudu, Justin Arunthamakun, Kathleen F Kopecky, Gregory P Milligan, Peter A McCullough, Thuy-Duyen Nguyen, Shahzad Shaefi, Megan L Krajewski, Sidharth Shankar, Ameeka Pannu, Juan D Valencia, Kenneth A Bauer, Sushrut S Waikar, Zoe A Kibbelaar, Ambarish M Athavale, Peter Hart, Shristi Upadhyay, Ishaan Vohra, Ajiboye Oyintayo, Adam Green, Jean-Sebastien Rachoin, Christa A Schorr, Lisa Shea, Daniel L Edmonston, Christopher L Mosher, Alexandre M Shehata, Zaza Cohen, Valerie Allusson, Gabriela Bambrick-Santoyo, Noor Ul Aain Bhatti, Bijal Mehta, Aquino Williams, Samantha K Brenner, Patricia Walters, Ronaldo C Go, Keith M Rose, Miguel A Hernán, Amy M Zhou, Ethan C Kim, Rebecca Lisk, Lili Chan, Kusum S Mathews, Steven G Coca, Deena R Altman, Aparna Saha, Howard Soh, Huei Hsun Wen, Sonali Bose, Emily A Leven, Jing G Wang, Gohar Mosoyan, Pattharawin Pattharanitima, Emily J Gallagher, Allon N Friedman, John Guirguis, Rajat Kapoor, Christopher Meshberger, Katherine J Kelly, Chirag R Parikh, Brian T Garibaldi, Celia P Corona-Villalobos, Yumeng Wen, Steven Menez, Rubab F Malik, Carmen Elena Cervantes, Samir C Gautam, Mary C Mallappallil, Jie Ouyang, Sabu John, Ernie Yap, Yohannes Melaku, Ibrahim Mohamed, Siddhartha Bajracharya, Isha Puri, Mariah Thaxton, Jyotsna Bhattacharya, John Wagner, Leon Boudourakis, H Bryant Nguyen, Afshin Ahoubim, Leslie F Thomas, Dheeraj Reddy Sirganagari, Pramod K Guru, Yan Zhou, Paul A Bergl, Jesus Rodriguez, Jatan A Shah, Mrigank S Gupta, Princy N Kumar, Deepa G Lazarous, Seble G Kassaye, Michal L Melamed, Tanya S Johns, Ryan Mocerino, Kalyan Prudhvi, Denzel Zhu, Rebecca V Levy, Yorg Azzi, Molly Fisher, Milagros Yunes, Kaltrina Sedaliu, Ladan Golestaneh, Maureen Brogan, Jyotsana Thakkar, Neelja Kumar, Michael J Ross, Michael Chang, Ritesh Raichoudhury, Akshay Athreya, Mohamed Farag, Edward J Schenck, Soo Jung Cho, Maria Plataki, Sergio L Alvarez-Mulett, Luis G Gomez-Escobar, Di Pan, Stefi Lee, Jamuna Krishnan, William Whalen, David Charytan, Ashley Macina, Anand Srivastava, Alexander S Leidner, Carlos Martinez, Jacqueline M Kruser, Richard G Wunderink, Alexander J Hodakowski, Juan Carlos Q Velez, Eboni G Price-Haywood, Luis A Matute-Trochez, Anna E Hasty, Muner M B Mohamed, Rupali S Avasare, David Zonies, David E Leaf, Shruti Gupta, Rebecca Karp Leaf, Rachel Rosovsky, Meghan E Sise, Erik T Newman, Samah Abu Omar, Kapil K Pokharel, Shreyak Sharma, Harkarandeep Singh, Simon Correa, Tanveer Shaukat, Omer Kamal, Wei Wang, Meghan Lee, Ian A Strohbehn, Jiahua Li, Ariel L Mueller, Roberta E Redfern, Nicholas S Cairl, Gabriel Naimy, Abeer Abu-Saif, Danyell Hall, Laura Bickley, Chris Rowan, Farah Madhani-Lovely, Vasil Peev, Jochen Reiser, John J Byun, Andrew Vissing, Esha M Kapania, Zoe Post, Nilam P Patel, Joy-Marie Hermes, Anne K Sutherland, Amee Patrawalla, Diana G Finkel, Barbara A Danek, Sowminya Arikapudi, Jeffrey M Paer, Peter Cangialosi, Mark Liotta, Jared Radbel, Sonika Puri, Jag Sunderram, Matthew T Scharf, Ayesha Ahmed, Ilya Berim, Jayanth S Vatson, George Karp, Shuchi Anand, Joseph E Levitt, Pablo Garcia, Suzanne M Boyle, Rui Song, Jingjing Zhang, Sang Hoon Woo, Xiaoying Deng, Goni Katz-Greenberg, Moh'd A Sharshir, Vadym V Rusnak, Muhammad Imran Ali, Anip Bansal, Amber S Podoll, Michel Chonchol, Sunita Sharma, Ellen L Burnham, Arash Rashidi, Rana Hejal, Eric Judd, Laura Latta, Ashita Tolwani, Timothy E Albertson, Jason Y Adams, Steven Y Chang, Rebecca M Beutler, Carl E Schulze, Etienne Macedo, Harin Rhee, Kathleen D Liu, Vasantha K Jotwani, Jay L Koyner, Chintan V Shah, Vishal Jaikaransingh, Stephanie M Toth-Manikowski, Min J Joo, James P Lash, Javier A Neyra, Nourhan Chaaban, Madona Elias, Yahya Ahmad, Rajany Dy, Alfredo Iardino, Elizabeth H Au, Jill H Sharma, Marie Anne Sosa, Sabrina Taldone, Gabriel Contreras, David De La Zerda, Hayley B Gershengorn, Alessia Fornoni, Salim S Hayek, Pennelope Blakely, Hanna Berlin, Tariq U Azam, Husam Shadid, Michael Pan, Patrick O'Hayer, Chelsea Meloche, Rafey Feroze, Kishan J Padalia, Jeff Leya, John P Donnelly, Andrew J Admon, Jennifer E Flythe, Matthew J Tugman, Emily H Chang, Brent R Brown, Amanda K Leonberg-Yoo, Ryan C Spiardi, Todd A Miano, Meaghan S Roche, Charles R Vasquez, Amar D Bansal, Natalie C Ernecoff, Sanjana Kapoor, Siddharth Verma, Huiwen Chen, Csaba P Kovesdy, Miklos Z Molnar, Ambreen Azhar, S Susan Hedayati, Mridula V Nadamuni, Shani Shastri, Duwayne L Willett, Samuel A P Short, Amanda D Renaghan, Kyle B Enfield, Pavan K Bhatraju, A Bilal Malik, Matthew W Semler, Anitha Vijayan, Christina Mariyam Joy, Tingting Li, Seth Goldberg, Patricia F Kao, Greg L Schumaker, Nitender Goyal, Anthony J Faugno, Greg L Schumaker, Caroline M Hsu, Asma Tariq, Leah Meyer, Ravi K Kshirsagar, Daniel E Weiner, Marta Christov, Jennifer Griffiths, Sanjeev Gupta, Aromma Kapoor, Savneek Chugh, Perry Wilson, Tanima Arora, Ugochukwu Ugwuowo

Abstract

Background: Hypercoagulability may be a key mechanism of death in patients with coronavirus disease 2019 (COVID-19).

Objective: To evaluate the incidence of venous thromboembolism (VTE) and major bleeding in critically ill patients with COVID-19 and examine the observational effect of early therapeutic anticoagulation on survival.

Design: In a multicenter cohort study of 3239 critically ill adults with COVID-19, the incidence of VTE and major bleeding within 14 days after intensive care unit (ICU) admission was evaluated. A target trial emulation in which patients were categorized according to receipt or no receipt of therapeutic anticoagulation in the first 2 days of ICU admission was done to examine the observational effect of early therapeutic anticoagulation on survival. A Cox model with inverse probability weighting to adjust for confounding was used.

Setting: 67 hospitals in the United States.

Participants: Adults with COVID-19 admitted to a participating ICU.

Measurements: Time to death, censored at hospital discharge, or date of last follow-up.

Results: Among the 3239 patients included, the median age was 61 years (interquartile range, 53 to 71 years), and 2088 (64.5%) were men. A total of 204 patients (6.3%) developed VTE, and 90 patients (2.8%) developed a major bleeding event. Independent predictors of VTE were male sex and higher D-dimer level on ICU admission. Among the 2809 patients included in the target trial emulation, 384 (11.9%) received early therapeutic anticoagulation. In the primary analysis, during a median follow-up of 27 days, patients who received early therapeutic anticoagulation had a similar risk for death as those who did not (hazard ratio, 1.12 [95% CI, 0.92 to 1.35]).

Limitation: Observational design.

Conclusion: Among critically ill adults with COVID-19, early therapeutic anticoagulation did not affect survival in the target trial emulation.

Primary funding source: None.

Conflict of interest statement

Disclosures: Disclosures can be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M20-6739.

Figures

Visual Abstract.. Early Anticoagulation in COVID-19
Visual Abstract.. Early Anticoagulation in COVID-19
Hypercoagulability may be a key mechanism of death in patients with COVID-19. This cohort study evaluated the incidence of venous thromboembolism and major bleeding in critically ill patients with COVID-19 and examined the observational effect of early therapeutic anticoagulation on survival.
Figure 1.. Flow diagram for target trial…
Figure 1.. Flow diagram for target trial emulation of therapeutic anticoagulation.
COVID-19 = coronavirus disease 2019; DVT = deep venous thrombosis; ECMO = extracorporeal membrane oxygenation; ICU = intensive care unit; PE = pulmonary embolism.
Figure 2.. Target trial emulation.
Figure 2.. Target trial emulation.
Survival in patients who received therapeutic anticoagulation in the first 2 days of ICU admission compared with those who did not. AC = anticoagulation; ICU = intensive care unit.
Figure 3.. Results of sensitivity and subgroup…
Figure 3.. Results of sensitivity and subgroup analyses.
Shown are the hazard ratios for survival according to early initiation of therapeutic AC versus no early initiation of therapeutic AC in the primary analysis, the sensitivity analyses, and across subgroups. AC = anticoagulation; HR = hazard ratio; ICU = intensive care unit.

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