Adult cardiac surgery and the COVID-19 pandemic: Aggressive infection mitigation strategies are necessary in the operating room and surgical recovery



## Central message
Aggressive infection mitigation strategies are necessary to safeguard our patients and healthcare workers during the COVID-19 pandemic.
The Centers for Disease Control and Prevention (CDC) recently published recommendations for the care of patients undergoing surgical procedures during the COVID-19 pandemic.Additional modifications provided by the American College of Surgeons offer further guidance for surgical patients and personnel.Both organizations have recommended significantly reducing or stopping elective cases and implementing logical, tiered general precautions.
The Society of Thoracic Surgeons COVID-19 Task Force and the Workforce for Adult Cardiac and Vascular Surgery published tiered patient triage guidance. [bib_ref] on behalf of The Society of Thoracic Surgeons COVID-19 Task Force and..., Haft [/bib_ref] Other suggestions from the American College of Surgeons to enhance safety for healthcare workersin the context of COVID-19 include the following:
1. Consider nonoperative management whenever it is clinically appropriate for the patient. 2. Complete testing as close to the planned operative date (preferably <48 hours) to lessen the risk that a patient becomes positive while waiting for a surgical procedure. 3. Avoid emergency surgical procedures during off hours, when possible, due to limited team staffing and the potential lack of optimal specialty specific expertise. 4. Perform aerosol-generating procedures (AGPs) [bib_ref] Aerosol generating procedures and risk of transmission of acute respiratory infections to..., Tran [/bib_ref] in confirmed or suspected COVID-19 patients while practicing enhanced droplet/contact precautions, including an N95 mask, eye protection, gown and gloves, or a powered air-purifying respirator. Examples of known and possible AGPs include:
a. Intubation, extubation, bag mask ventilation, noninvasive ventilation (continuous positive airway pressure and bilevel positive airway pressure), airway suctioning, nebulizer therapies, bronchoscopy, chest tube insertion, thoracotomies, and pleural procedures b. Electrocautery of blood or any other body fluids 6 c. Endoscopy 5. Defer nonurgent cardiovascular testing. 6. Distinguishing COVID-19 from other respiratory infections will be challenging; therefore, interventions will need to be applied broadly and not limited to patients with confirmed COVID-19.While helpful, these guidelines do not provide the granular guidance needed to address important aspects of the surgical management of cardiac surgical patients. In particular, there will remain a certain volume of patients who will still require urgent and emergent operations during this pandemic.
At time of writing this document, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the novel coronavirus associated with COVID-19 disease, has been associated with at least a 6% mortality in the United States in those patients with a confirmed diagnosis.The virus is well equipped with several virologic, epidemiologic, and clinical features that have contributed to its ability to rapidly spread through a global population. Specifically, a substantial number of asymptomatic or presymptomatic infections, with or without mild symptoms, are key to its effective dissemination throughout populations, including to healthcare providers. [bib_ref] Substantial undocumented infection facilitates the rapid dissemination of novel coronavirus (SARS-CoV-2), Li [/bib_ref] At times of documented or assumed community spread of COVID-19, it is reasonable to suspect that all patients could be carriers of the virus. As such, all patients should be considered COVID-19 suspects, regardless of testing availability or results, and all patients should be treated equally with precautions similar to those used in COVID-19-confirmed cases.
This approach is similar to the concept of universal precautions. This level of safety may not be required if community transmission and the burden of cases is low in specific areas. However, to minimize infectious risk to healthcare providers of patients undergoing cardiac surgical procedures in the preoperative, intraoperative, and postoperative period, additional detailed protective strategies are suggested. These are guidance recommendations during a pandemic surge for all patients until the supply chain for personal protective equipment (PPE) is restored and local COVID-19 disease burden is substantially reduced.

## Guidance recommendations
1. Patients should be transferred directly to the operating room (OR), without stopping in the preoperative or postanesthesia care unit areas, to minimize exposure to other patients, staff, and other environments. 2. "COVID-19 precautions" signs should be posted on all doors to the OR suite to inform staff of potential risks and minimize exposure. 3. The OR should remain positive pressure, but the surrounding rooms (ie, anteroom[s]) must maintain a strict negative pressure ventilation system at more than A2.5 Pa at 12 or more air changes per hour. 9 4. All OR staff are required to practice enhanced droplet and contact precautions in the OR at all times. This includes the use of N95 respirator, eye protection, gown, and gloves. Given the possibility of false-negative testing (10%-30%), [bib_ref] Evaluating the accuracy of different respiratory specimens in the laboratory diagnosis and..., Yang [/bib_ref] 
[formula] Ig 14 immunoglobulin OR 14 operating room PPE 14 personal protective equipment SARS-CoV-2 14 severe acute respiratory syndrome coronavirus 2 TEE 14 transesophageal echocardiography [/formula]
Anesthesiologists recommends that all anesthesia professionals should use PPE appropriate for AGPs for all patients during all diagnostic, therapeutic, and surgical procedures when working near the airway.We would broaden this recommendation to include all OR personnel. 5. If N95 masks are to be reused (though not optimal) the CDC recommends a 5-day period of drying 12 or preferably decontaminated using ultraviolet germicidal irradiation, vaporous hydrogen peroxide, or moist heat by autoclaving. 12,13 6. If a powered air-purifying respirator is used as an alternative to an N95 respirator and eye protection, practitioners should be cautioned that these devices may reduce the clarity of surgical loupes and positioning of headlights. 7. A donning-and-doffing-trained observeris highly recommended because most nosocomial spread of COVID-19 occurs during this critical period. [bib_ref] Self-contamination during doffing of personal protective equipment by healthcare workers to prevent..., Suen [/bib_ref] Ongoing donning-and-doffing simulation training should be regularly performed for continual refinement of safety processes. 8. Limit entry/exit to a single OR entrance. Keep all OR doors closed as much as possible, and limit staff entry/reentry to keep OR pressures and air exchanges regulated. 9. Before AGPs are performed, OR personnel must ensure that no more than the minimal number of staff required to safely achieve the procedure are present in the room. 10. During induction and endotracheal intubation, it is recommended that the anesthesiologist:
a. Be the most experienced available operator with the highest probability of first-pass intubation. b. Limit the number of staff in the OR to the minimum needed to safely intubate (1 anesthesiologist plus 1 or 2 assistants). c. At the discretion of the anesthesiologist, video laryngoscopy may be chosen over direct visualization to decrease the risk of droplet transmission. d. Preoxygenate with 100% inspired oxygen and avoid bag-mask ventilation unless absolutely necessary. 11. After AGPs, including intubation, additional OR personnel should wait 30 minutes before entering the room (this is dependent on the efficiency of the air exchange in each OR suite; see point 3 above). 12. Intraoperative staffing for the surgical case should be minimized to the minimal number needed to safely and efficiently complete the procedure. [bib_ref] N95 mask decontamination using standard hospital sterilization technologies, Kumar [/bib_ref]. Staff relief for breaks should be provided only as necessary to preserve PPE and decrease the number of staff exposed and reentries. 14.
Smoke evacuation of electrosurgical devices should be used to minimize staff exposure to surgical smoke. [bib_ref] Awareness of surgical smoke hazards and enhancement of surgical smoke prevention among..., Liu [/bib_ref] 15. Patients should preferably recover in a negativepressure isolation room when resources permit (in the postanesthesia care unit or intensive care unit). If negative-pressure isolation rooms are unavailable, consider early recovery in the OR before transfer to a single patient room. 16. After the patient has left the OR, the OR should be closed for an appropriate standoff period to achieve greater than 99.9% aerosol clearance. The amount of time that aerosols stay suspended in the air will depend on a number of factors, including the size of the room, the number of air changes per hour, how long the patient was in the room, whether the patient was coughing or sneezing, and whether an AGP was performed. General guidance on clearance rates under differing ventilation conditions is available from the CDC.17. After the standoff period, the OR suite must be cleaned using routine procedures with United States Environmental Protection Agency-approved hospital disinfectant. 18. Operations should be performed by the most experienced available surgeons and assistants to limit exposure time in the OR. Junior residents and other learners should not be exposed unless absolutely necessary. 19. Strong consideration to surgical approach and technique must be considered to optimize patient outcomes while minimizing exposure risk to providers. Use of laparoscopic or video-assisted thoracoscopic procedures should be avoided when possible due to risk of aerosolization from CO 2 insufflation systems with inadvertent lung injury. 20. Limit all routine preoperative and postoperative laboratory testing, imaging, and procedures to minimize personnel exposure. 21. COVID-19 repeat testing is only required in postoperative patients when symptoms or signs of COVID-19 develop. Rapid COVID-19 testing is preferred when available. 22. In the event of cardiac arrest or other medical emergency, all patients must continue to be treated as suspected or confirmed COVID-19 cases. This requires strict adherence to enhanced contact and droplet precautions. No patient interaction should be permitted before full PPE is donned. This likely represents an uncomfortable paradigm shift for surgeons accustomed to "jumping into lifesaving patient interactions with little regard to infectious risk." 23. For a cardiac arrest in the intensive care unit, only 1 provider should provide cardiopulmonary resuscitation while medications are administered. Cessation of advanced cardiac life support is at the discretion of the provider, but prolonged resuscitative efforts should be avoided due to futility and risk. [bib_ref] In-hospital cardiac arrest outcomes among patients with COVID-19 pneumonia in Wuhan, Shao [/bib_ref] 24. Transesophageal echocardiography (TEE) in an intubated, anesthetized patient has never been demonstrated to generate aerosols. However, many societies have classified TEE as an AGP. Clinicians should weigh the necessity of placing a TEE in each cardiac surgical patient against the theoretical concern of generating aerosols. If performed, all staff should wear an N95 mask. The most experienced echocardiographer should perform the examination, including probe insertion and removal. 18

## Covid-19 testing
There is accumulating evidence indicating that a substantial fraction of COVID-19-infected individuals are asymptomatic. [bib_ref] Evidence of SARS-CoV-2 infection in returning travelers from Wuhan, China, Hoehl [/bib_ref] A study of skilled nursing facility residents infected with COVID-19 demonstrated that half were asymptomatic or presymptomatic at the time of contact tracing evaluation and testing. [bib_ref] Asymptomatic and presymptomatic SARS-CoV-2 infections in residents of a long-term care skilled..., Kimball [/bib_ref] In a population-based study in Iceland, 43% of the participants who tested positive reported having no symptoms. [bib_ref] Spread of SARS-CoV-2 in the Icelandic Population, Gudbjartsson [/bib_ref] A study of 215 pregnant women admitted for delivery in New York City found 15% were COVID-19 positive, 88% of whom were asymptomatic. [bib_ref] Universal screening for SARS-CoV-2 in women admitted for delivery, Sutton [/bib_ref] Virologic studies have demonstrated viral RNA and viable virus among persons with asymptomatic and presymptomatic infection. [bib_ref] Evidence of SARS-CoV-2 infection in returning travelers from Wuhan, China, Hoehl [/bib_ref] [bib_ref] Asymptomatic and presymptomatic SARS-CoV-2 infections in residents of a long-term care skilled..., Kimball [/bib_ref] [bib_ref] SARS-CoV-2 viral load in upper respiratory specimens of infected patients, Zou [/bib_ref] If a high-fidelity, rapid point-of-care testing system is available, providers could consider screening preoperative patients immediately before a surgical procedure if time permits within a 24-hour window, particularly in areas of high COVID-19 disease burden. Positive screening tests should lead to reconsideration of the risks and benefits of proceeding with the planned surgical procedure. These patients may be in the presymptomatic or early symptomatic phase of infection and are likely at heightened risk of adverse outcomes after an operative procedure. In a retrospective cohort study of 34 patients who were unintentionally scheduled for elective operations during the incubation period of COVID-19, the mortality rate was 20%. [bib_ref] Clinical characteristics and outcomes of hospitalised patients with COVID-19 treated in Hubei..., Liang [/bib_ref] However, negative screening tests must be interpreted with caution, particularly in the setting of (1) low pretest probability, (2) typically low viral titers in the asymptomatic phase, and (3) the possibility of false-negative results. If clinical suspicion for COVID-19 remains due to exposure history, active symptoms, high prevalence of circulating community infections, or other clinical factors, repeat testing may be indicated during the postoperative course.

## Serologic immunity
After viral infections, an immunoglobulin (Ig) M immune response occurs, which then diminishes within a few weeks. The IgG and IgA immune response occurs simultaneously, producing more specific and longer-acting immunity.Testing patients' serostatus could be an important tool to determine whether patients have mounted prior immunity from natural infection, reducing the likelihood of current COVID-19 colonization. The prospect of testing providers for serologic immunity to COVID-19 is also promising if the presence of antibodies confers immunity to future infection, because providers with acquired immunity could be selected to care for COVID-19 suspected or confirmed patients.
Unfortunately, serologic testing and capacity are currently limited and require further scientific evidence to support their use in screening healthcare workers. Important studies are underway to determine the pattern of antibody development after COVID-19 infection, whether antibodies confer immunity to future infections, whether specific antibody titers determine the level of protection, and the duration of conferred immunity.
Similar coronavirus outbreaks demonstrated that survivors developed robust immunity after natural infection. The 2003 severe acute respiratory syndrome outbreak elicited an immunity that was protective for up to 3 years. [bib_ref] Duration of antibody responses after severe acute respiratory syndrome, Wu [/bib_ref] Until more data emerge supporting the widespread adoption of antibody testing, 29 strict infection prevention and control policies are required to enhance the safety of patients and providers.

# Conclusions
At the present time, we urge all healthcare organizations providing cardiac surgical procedures in regional environments of widespread COVID-19 disease to consider adopting these aggressive mitigation strategies (1) to create a safe environment that protects our patients from acquiring or transmitting COVID-19 and (2) to protect members of our surgical and postoperative provider teams. We all look forward to the near future when elective surgical procedures can be resumed as the threat of this virus wanes and capacity permits. However, until that time, and in an effort to hasten its arrival, the aforementioned protocols should become standard of care.
Rakesh C. Arora has received an unrestricted educational grant from Pfizer Canada Inc.