recommended to stratify patient risk in delaying surgery beyond seven weeks on a personalized basis (11). In one systematic review including >250,000 patients, more than half had post-acute sequelae of COVID-19 at six months follow-up (12). Clearly, there is a significant need to risk stratify this patient population on an individualized basis. The most recent American Society of Anesthesiologists (ASA) and Anesthesia Patient Safety Foundation (APSF) joint recommendation for the delay of surgery have been divided into four blocks of time based upon the symptoms and severity of acute COVID-19 illness: • “Four weeks for an asymptomatic patient or recovery from only mild, non-respiratory symptoms • Six weeks for a symptomatic patient (e.g., cough, dyspnea) who did not require hospitalization • Eight to 10 weeks for a symptomatic patient who is diabetic, immunocompromised, or hospitalized • Twelve weeks for a patient who was admitted to an intensive care unit due to COVID-19 infection” The ASA and APSF joint recommendation further states: “These timelines should not be considered definitive; each patient’s preoperative risk assessment should be individualized, factoring in surgical intensity, patient co-morbidities, and the benefit/risk ratio of further delaying surgery” (13). Specifically, these recommendations have not considered the differing degrees of coagulopathy associated with COVID-19 variants. Additionally, there is little guidance on elective surgery for patients afflicted with Long COVID, and there are few proposals for preoperative laboratory measurements (e.g., D-dimer, fibrinogen, ferritin, lactate dehydrogenase (LDH), and other clinical and laboratory markers of severity of disease) to guide surgeons and anesthesiologists for the appropriate timing of surgery (14, 15). Likewise, sparse guidance exists for the postoperative thromboprophylaxis of this patient group. In a large study of 11,249 patients from the first COVID-19 surge in the Spring of 2020 in New York City, 1.7% of all patients discharged from the hospital had VTE or arterial thromboembolism (16). This study also reported that prophylactic anticoagulation with either enoxaparin or rivaroxaban engenders a 46% reduction in clotting disorders (16). However, the unique pathophysiological aspect of COVID-19 pneumonitis is that these patients may bleed and clot at the same time when anticoagulated (17). It was reported that 1.73% of discharged patients suffered major bleeding within 90 days of discharge while only 13.2% of the entire cohort was administered thromboprophylaxis (16). Together these findings offer surgeons the opportunity to familiarize themselves with the unique hemostatic derangement of CAC affecting postoperative outcomes worldwide. A basic flow chart for triaging acute and convalescent COVID-19 patients based upon recent ASA and surgical guidelines for the timing of surgery and postoperative VTE prophylaxis is presented in Figure 1. Clear data demonstrates unvaccinated individuals with COVID infection procure a higher risk of thrombosis and more severe illness. Breakthrough infections in vaccinated individuals have less thrombotic risk and lower risk of severe illness (27). Following the ASA guidelines, patients’ length of delay for surgery should be based on the severity of illness regardless of vaccination status. The impact of COVID-19 on immune system-related complications in surgical patients is a crosstalk between immunology and coagulation at the level of the endothelium. This is more than a theoretical concept; rather, it is an important pathophysiologic understanding of the unique challenges of operating on patients who have either recent or remote infections with the SARS-CoV-2 virus. Few guidelines exist concerning the timing and nature of this dual threat of bleeding and clotting that occur in a surgical patient with COVID-19 (28, 29). This review will address the pathophysiologic underpinnings of COVID-19 as it relates to surgical timing and thromboprophylaxis, followed by a specific application of these immune-thrombotic changes to perioperative and postoperative management of patients. COVID-19-ASSOCIATED COAGULOPATHY (CAC) Recent consensus and guidelines exist, but they lack granularity to assist the surgeon for optimizing the timing of elective surgery and guiding postoperative thromboprophylaxis for their individual convalescent COVID-19 patients. The longterm effects of COVID-19 infection are still under investigation. Hence, there are limited studies or specific guidelines aiding the surgeon in weighing risks and benefits of elective surgery for patients post-recovery from COVID-19. Persistent complications of COVID-19 infection after recovery are a product of the vast endothelial damage induced by SARS-CoV-2 (29). It is pertinent for the surgeon and anesthesiologist to understand the mechanisms of this endotheliitis to individualize care for their convalescent COVID-19 patients in this time of limited evidence-based guidance. Pathophysiology of CAC: A Labile Balance Between Fibrinolysis and Fibrinolytic Shutdown Immuno-thrombosis is often described as the dysregulated interaction between innate immunity and coagulation (30–32). A reported 30-80% of COVID-19 ICU patients endure thrombotic complications during their clinical course (33–36). The most common thrombotic complication in COVID-19 patients is VTE, which occurs in 15-85% of patients (37). Although the exact mechanism behind CAC is poorly understood, endotheliitis likely incites the hypercoagulable state (Figure 2) (38–42). The SARS-CoV-2 virus directly invades endothelial cells through the angiotensin converting enzyme 2 (ACE2) receptor. This leads to localization of viral inclusion bodies in the lungs, liver, small intestines, and kidneys, shedding of endothelial glycocalyx proteins, and decreases in the level of heparanase-2. This results in a Bunch et al. COVID-19 Immuno-Thrombosis and Surgery Frontiers in Surgery | www.frontiersin.org 3 2022 | Volume 9 | Article 889999 JULY 2022 | The Surgical Technologist | 303
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