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Intraoperative Measures to Reduce the Risk of COVID-19 Transmission During Minimally Invasive Procedures: A Systematic Review and Critical Appraisal of Societies’ Recommendations

Supplemental Digital Content is available in the text.

S evere acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is responsible for a worldwide epidemic, which was declared as a pandemic by the World Health Organization on March 11, 2020. The current evidence suggests the primary source of transmission of SARS-CoV-2 is through respiratory droplets (particles > 5 to 10 μm in diameter) 1 from infected people and through contact with contaminated surfaces. 2 There is growing evidence that coronavirus 2019  infection may also occur from airborne exposure to the virus under certain circumstances. 3 Given that the transmission mechanism of this virus is still largely unknown, concerns have been raised regarding the possibility of virus transmission to the operative room (OR) staff during surgical procedures. In particular, Cahmpault et al 4 questioned the potential creation of aerosols containing contaminated material from CO 2 leakage, as well as the creation of surgical smoke from energy devices during laparoscopic procedures.
Although the risk of viral transmission in the OR was not unknown to experts, the use of measures to address it before the onset of the COVID-19 pandemic were either lacking or not widely adopted. The sudden spread of the disease put significant pressure on surgical societies to quickly address the safety issues related to performing surgical procedures in this environment. For this reason, initial recommendations were issued, in particular leveraging the initial experiences from China, to stop elective surgery and to avoid laparoscopic procedures, favoring an open approach. The Royal College of Surgeons and associated societies updated their recommendations, suggesting that proponents of laparoscopy during the COVID-19 pandemic understand the potential risks and the need for risk mitigation strategies. The recommendations included the use of technological protection and enhanced personal protective equipment (PPE). Societies continued to suggest that laparoscopy can be cautiously reestablished when mitigation criteria were met, OR teams were satisfied with the safety measures and when the teams considered the benefits of laparoscopy outweigh the risks in their local OR set-up. 5 Other recommendations, along with expert opinion articles on which measures to adopt to reduce the risk of viral transmission during laparoscopic and robotic procedures have been published since the beginning of the pandemic. Areas which were frequently discussed include the adoption of PPE, workflow and organizational protocols, procedure prioritization, pneumoperitoneum management (including CO 2 leaks), and the use of energy devices, and smoke evacuation technologies.
Currently, there is no evidence of the presence of SARS-CoV-2 in surgical smoke or in the aerosolized CO 2 from laparoscopic procedures, but for the sake of safety and in lieu of lacking evidence, recommendations were set assuming the presence of the virus in these mediums. Many recommendations were based on opinion or a thought process, rather than evidence.
Laparoscopy has been demonstrated to bring significant advantages over the open approach, 6 even more so during a pandemic, since it may reduce hospital length of stay and, potentially, postoperative complications. For this reason, it is important to identify effective measures to reduce the risk of viral transmission to the OR staff, based on scientific evidence.
The aim of this systematic review is to identify, summarize and critically appraise recommendations from surgical societies focusing on intraoperative measures to reduce the risk of SARS-CoV-2 transmission to the OR staff.

Search Strategy
A comprehensive literature search was performed according to the 2009 Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) guidelines. 7 To identify published articles reporting recommendations on intraoperative measures to reduce the risk of SARS-CoV-2 transmission to the OR staff during MIS procedures, a combination of keywords (MeSH terms and free text words) including ("COVID-19" OR "SARS-CoV-2" OR "Coronavirus" OR "coronavirus infections") AND ("laparoscopy" OR "laparoscopic surgery" OR "robotic surgery" OR "minimally invasive surgery" OR "MIS" OR "minimally invasive procedures") AND ("recommendations" OR "guidelines" OR "position" OR "statement") were used to search Medline, Embase, and Google Scholar databases (search strategies are provided in the Supplementary material, Supplemental Digital Content 1, http://links.lww.com/ SLE/A293). The search was supplemented to include pertinent references from the retrieved articles as well as searches of additional relevant records on COVID-19 resource websites from Surgical Associations and Societies to identify recommendations which were not published in journals. The search included publications from October 1, 2019 through November 20, 2020.

Eligibility Criteria
Articles were eligible for inclusion if they contained societies' guidelines or recommendations detailing measures to adopt during minimally invasive abdominal surgery (including laparoscopy and robotic abdominal surgery) to reduce the risk of SARS-CoV-2 transmission to the OR staff. The exclusion criteria were as follows: (1) not focused on laparoscopy or robotic abdominal surgery; (2) not containing official recommendations from a surgical society involving OR practices during the COVID-19 pandemic; (3) expert opinion articles; and (3) language other than English.

Information Sources
The search yielded 413 articles, after exclusion of duplicates. Two authors independently identified and reviewed the titles and abstracts. For an article to be excluded, both reviewers had to agree that the study was not relevant. One or more of the following areas or recommendations had to be present in the article to include it in the analysis: recommendation on whether to perform minimally invasive surgery (MIS), selection of surgeon to perform MIS, use of energy devices, use of smoke evacuation systems, recommendation on access and on creation and maintenance of pneumoperitoneum. After reviewing the titles and abstracts, 103 papers were identified as potentially eligible for inclusion. After a full-text review, 33 documents were deemed eligible and were included. The Preferred Reporting Items for Systematic Reviews and Meta-analysis flow diagram is shown in Figure 1.

Data Extraction
Two independent reviewers extracted relevant recommendations from each guideline. Disagreements concerning data extraction were resolved by discussion and consensus. Thereafter, a recommendation matrix was constructed. The following variables were extracted from the articles: list of authors, title of the article, name of the society, publication date, country, type of surgery, recommendation on the surgeon(s) to involve in MIS procedures, the choice between MIS or open approach, the use of energy devices, the use of smoke evacuation systems, on any measure to limit CO 2 escape from trocars, and on creation and maintenance of pneumoperitoneum.

Data Synthesis and Analysis
A preliminary synthesis was performed of the extracted data to categorize and itemize the different types of recommendations. The results were then summarized in a narrative synthesis.

Selection of Surgical Staff
Thirteen recommendations suggested that the selection of the surgeon performing MIS procedures is critical. 9,[11][12][13]16,25,26,28,29,32,33,35,39 All 13 also recommended that senior, trained laparoscopic surgeons should perform the procedures. OSSI suggested that a procedure-specific "time out" checklists be developed and that 2 trained surgeons pair up to perform the procedures. 9 ISDS proposed that only easy laparoscopic cases should be performed, 25 while SRED/ARCE recommended that laparoscopy should be performed based on the degree of competence of the operating team, institutional protocols, and the availability of specific equipment (Table 1). 33

Management of Peritoneum
All documents provided recommendations on the safe evacuation and management of the pneumoperitoneum. The references suggested not to evacuate the pneumoperitoneum for specimen extraction, for trocar re-insertion and at the end of the procedure without suction (entirely aspiration) or a filtered system. The Joint Statement of Gynecologic Societies recommends avoiding rapid desufflation or loss of pneumoperitoneum (Table 2). 10 Twenty-one societies also recommend using the lowest intra-abdominal pressure without compromising surgical exposure or patient safety. 9,10,12,14,16,19,20,[22][23][24][25][26][27][28][29][30][32][33][34][35]39 Four societies recommend an intra-abdominal pressure of 10 to 12 mm Hg, 10,30,34,35 2 societies a pressure ≤ 12 mm Hg, 12,29 the Italian Society of Bariatric Surgery 24 suggests a pressure of <10 mm Hg, the International Federation for the Surgery of Obesity and Metabolic Disorders-Latin American Chapter 14 indicates pressures from 10 to 15 mm Hg, while the Philippine Association of Laparoscopic and Endoscopic Surgeons 26 suggests a pressure of 8 to 10 mm Hg. Three societies recommend avoiding the use of 2-way insufflators, 23,28,35 while one of the societies suggested the use of intelligent integrated flow systems. 23 Seven documents indicated that Trendelenburg position be reduced or avoided which would reduce blood return to the pulmonary area. 16,24,26,29,30,36,37 The Obesity and Metabolic Surgery Society of India recommends using the most familiar technique for pneumoperitoneum creation, but to avoid open techniques. 9

Use of Energy Devices
Twelve articles advise to minimize 11,12,18,20,24,29,[35][36][37]39,40 or avoid 13 the use of electrocautery and energy devices due to the risk of the potential presence of viral particles in the smoke plume. Five of these recommendations, 20,35,37,39,40 together with 8 other recommendations 9,10,19,22,23,26-28 additionally suggest lowering the power setting on electrocautery and ultrasonic devices for the same reason. Minimization of desiccation times is also recommended by 8 documents (Table 2). 10,19,24,27,30,[35][36][37] Several articles also differentiate among alternative types of energy devices, claiming that 1 type of energy might be safer than others with respect to the creation of surgical smoke, and some also suggest specifically not to use ultrasonic or advanced bipolar devices. The Turkish Association of Endocrine Surgeons 13 suggests that the use of bipolar electrocautery can produce less smoke than monopolar cautery or ultrasonic devices, the Society of European Robotic Gynaecological Surgery advises to avoid the use of ultrasonic sealing and if possible, to use electrothermal bipolar vessel sealing. 22 The EAU recommendations 23,28,32 indicate that the low-temperature aerosol from ultrasonic scalpels or scissors cannot effectively deactivate the cellular components of virus in patients compared with conventional diathermy. The Indonesian Society of Digestive Surgeons recommends that ultrasonic dissectors and advanced bipolar devices should be minimized, as they can lead to particle aerosolization, 25 while the Society for Robotic Surgery 27 also claims that ultrasonic devices create significant aerosol without desiccation of tissue, and potentially viral release and suggest they should be used judiciously. For the Indian Association of Pediatric Surgeons, 36 the various energy sources lead to different sizes of particles, electrocautery, and LASER having the smallest, hottest particles and ultrasonic devices larger, cooler particles, suggesting that the former are less dangerous. The European Hernia Society 38 advises to avoid energy devices which produce more particles (eg, ultrasonic devices) and, finally, the International Society for Gynecologic Endoscopy 39 emphasizes that the  25 Laparoscopic procedures should be undertaken by the most experienced surgeon. Choose only easy laparoscopic cases In the absence of convincing data, the safest approach may be the one that is most familiar to the surgeon and reduces the operative time. If the recommended standard cannot be fulfilled, it is best not to perform laparoscopic procedure PALES 26 Limit laparoscopic procedure to the most proficient surgeon theoretical risk of increased smoke and particle dispersion is associated with the high frequency oscillating mechanism of ultrasonic devices.

Management of Surgical Smoke and Pneumoperitoneum Desufflation
All documents reported recommendations regarding measures to evacuate surgical smoke and on how to desufflate the pneumoperitoneum. All the societies, except the EAU Pediatric suggest the use of a closed smoke evacuation system connected to a filter to evacuate smoke and/or pneumoperitoneum before port exchange or specimen retrieval or at the end of the procedure (Table 2).

DISCUSSION
The spread of the COVID-19 pandemic has exerted significant pressure on the health care systems worldwide. It also has impacted both elective and emergent surgical activities-which were either halted or substantially reduced. Surgical activities were affected due to the lack of information around the possibility of viral transmission to patients, surgeons and OR staff during surgical procedures.
MIS procedures such as laparoscopy and abdominal robotic surgery are aerosol-generating procedures due to the creation and maintenance of pneumoperitoneum through insufflation of the abdominal cavity with CO 2 . For this reason, some societies were pressed to release recommendations during the first phase of the pandemic and suggested stopping MIS approaches in favor of open. In the following weeks and months, several recommendations were issued suggesting, instead, to consider using MIS approaches while adopting additional methods to minimize aerosolization of CO 2 , reducing or evacuating surgical smoke and enhancing PPE measures. Even if most of these methods had already been flagged during previous viral outbreaks, mainly for human immunodeficiency virus (HIV), 41 they were either underestimated or adopted by only a few.
Considering the urgency to ensure the health and safety of the OR staff, most of these recommendations were based in part on scientific evidence and relied mostly on a theoretical basis. Some recommendations to use certain devices over others were only based on either personal beliefs of the authors or a misinterpretation of available evidence. This systematic review highlighted that societies are in agreement with most of the recommendations.

MIS/Laparoscopic/Robotic Approaches Versus Open Approach
During the very first phase of the pandemic, some medical societies recommended not performing MIS  39 The most experienced, proficient and knowledgeable surgeon available should perform the procedure No robust evidence of increased risk of viral transmission during laparoscopy. All precautions must be taken during this time until more evidence becomes available USANZ 40 -   5 This recommendation was based the potential transmission of SARS-CoV-2 to the OR staff. As the pandemic continued, almost all societies made the recommendation to adopt a series of measures to reduce the potential risk of viral transmission to the OR staff in support of performing MIS procedures. 20 These later recommendations shifted to consider both the safety of the OR staff, as well as the patient. It is therefore acceptable to utilize MIS approaches whenever they are indicated, provided additional safety measures are implemented.

Selection of Surgical Staff
Different recommendations advised allowing only senior staff to perform MIS procedures. This rationale is based on the notion that experienced surgeons are able to complete demanding laparoscopic and robotic surgeries in significantly less time. Wang et al, 42 found, however, that the level of seniority does not have a substantial impact on operative times for postgraduate surgeons. The opposite was observed by Kauvar et al, 43 where junior residents experienced slower operative times. Other techniques, such as mental training, digital simulators and robotic technologies are becoming helpful for relatively inexperienced surgeons. [44][45][46][47]

Management of Peritoneum
A common recommendation is to reduce the pressure in the pneumoperitoneum to a minimum which will lessen CO 2 leakage from trocars. Most of the recommendations suggest pressure levels which are regularly used in laparoscopic procedures (ie, 10 to 15 mm Hg). Rohloff et al, 48 showed that a lower insufflation pressure with CO 2 at 8 mm Hg may reduce postoperative ileus without any other negative outcome. This finding was further supported and supplemented in several other studies which showed better postoperative recovery (decreased ileus rates), 49 reduced pain and hospital stay. 50

Trocars
The COVID-19 pandemic has added a new dimension to the debate on trocar safety, injecting fear of contamination from gas leakage into the OR staff on the frontline. Rather than identifying a new risk, the COVID crisis highlighted how the risk of staff contamination during laparoscopy has been dealt with. 51 Practically, SARS-CoV-2 is not the only infectious agent which should be considered and there is no reason to distinguish this new virus from prior recommendations which were established pre-COVID-19 pandemic.
On the basis of the perceived gas containment, balloon tip trocars have become more popular. Surgical society guidelines and recommendations have mentioned this property of the balloon trocar, but have not included support for their recommendations. 52,53 As suggested by several recommendations, CO 2 leakage at the insertion point can be minimized with attention focused on a precise size of the incision. Port placement is often left to junior level surgeons who use varying techniques ranging from a simple eye-ball approach to a meticulous marking of an incision on the skin. High end ports propose a feature ensuring adequate skin incision size: the 45-degree shape of the cannula end allows for printing an oval mark on the skin, the long diameter of which represents the optimal size for low gas leak, low force insertion and   51 Ensuring all ports not in use are closed prior insertion or insufflation, a measure which is present in a number of societies' recommendations, are easy to miss. A simple "check-list" approach could certainly help prevent these types of events related to trocars. Digital workflow, an emerging OR technology, includes dynamic checklists and reduced variability in the OR. 55

Use of Energy Devices
Most recommendations on the use of energy devices focused on reducing use, as well as lowering the power setting when using. Some suggested avoiding the use of ultrasonic devices, claiming they produce a low-temperature plume which may not inactivate the virus and thus contain potentially viable virions. These recommendations were based on evidence on other viruses (such as human papilloma virus, hepatitis B virus, and HIV) or a thought process.
Different studies reported the presence of viruses in the surgical smoke produced by energy devices, in particular human papilloma virus, 56 hepatitis B virus, 57 and HIV. 58,59 While some of these studies demonstrated the presence of a virus in an in vitro setting, 58,59 others did demonstrate the presence of a virus in the surgical smoke produced in an OR. 56,57 The only reported viral transmission to the OR staff was from surgeons operating on genital warts using a laser beam in an open setting, resulting in several OR staff cases of laryngeal papilloma. 60,61 There are no reports to date of viral infection from the use of energy modality to the OR team performing laparoscopic or robotic procedures. In addition, there have not been reports nor evidence of transmission to the OR staff during outbreaks of similar airborne viruses. 62 Some recommendations during the pandemic suggested surgeons use bipolar energy instead of ultrasonic devices, based on the hypothesis that the latter may produce a cooler plume which is unable to deactivate the virus and thus will contain more viable virions. Ultrasonic shears do produce a cooler, vapor-like plume but its temperature at the site of action is significantly higher than radiofrequency devices. 63 There are contrasting results on the presence of viable cells in the plume of ultrasonic devices. A study by Nduka et al 64 demonstrated, in an experimental setting, that large quantities of cellular debris were trapped in the plume from both ultrasonic hook and monopolar with a needle probe after ablation of tumors, but no viable cells were isolated from the smoke of either device. However, In et al 65 captured and injected into mice the smoke generated from an ultrasonic device activated on cancer cells in a petri dish. Of the 40 injection sites, 16 (40%) grew cancer cells identical to those on the petri dish. On the other hand, no other studies have evaluated the content of infectious material found in the plume from ultrasonic devices.
A recent study by Hayami et al 63 evaluated the temperature of the steam from an ultrasonic shear and compared it to an advanced bipolar device. The authors performed an ex vivo animal study and tested the devices in 4 different combinations of device and muscle conditions, including dry-dry, dry-wet, wet-dry, and wet-wet. In this study, bipolar devices produced cooler surgical smoke which is also theoretically incapable of inactivating a virus.
Emam and Cuschieri 66 reported opposite results when they compared 2 ultrasonic devices at power levels 3, 4, and 5 in a random fashion in preclinical porcine model. After continuous ultrasonic dissection for 10 to 15 seconds at power level 5, the authors observed that the zone around the jaws which exceeded 60°C was measured at 25.3 and 25.7 mm for the 2 different ultrasonic devices tested. At this power setting with an activation time of 15 seconds, the temperature 1.0 cm away from the tips of the instrument exceeded 140°C. It was observed that temperatures 1 cm away from the jaws of both instruments were all above 80°C for power settings level 4 and level 5. A recent study from Dalli et al 67 evaluated gas leaks from the handles of an advanced bipolar device, a robotic energy device and an ultrasonic device. A video produced by these authors demonstrated significant gas leaks though the handles of the advanced bipolar and the robotic devices, however there was only a small amount of leakage through the handle of the ultrasonic device.

Management of Surgical Smoke and Pneumoperitoneum Desufflation
All documents from surgical societies suggest the use of a closed smoke evacuation system connected to a filter to evacuate smoke and/or pneumoperitoneum before port exchange or specimen retrieval or at the end of the procedure. Considering that only a limited number of health care facilities have smoke evacuation systems with an ultra-low particulate air (or high-efficiency particulate air) filter, some recommendations indicate using suction to evacuate smoke or CO 2 , either through a normal aspiration system or through a filter. A limited number of recommendations call out the use of specific systems such as Airseal 27,40 or PneumoClear. 40 The AirSeal system (SurgiQuest Inc., Milford, CT) is a novel class of valve-free insufflation system that enables a stable pneumoperitoneum with continuous smoke evacuation and CO 2 recirculation during surgery. 68 Even though different studies demonstrated some advantages of this system on operative time and stability of pneumoperitoneum, 69 there were also contrasting results. 70

CONCLUSIONS
The COVID-19 pandemic has significantly impacted the health care system globally. While in the first phases of the viral outbreak the lack of information on the epidemiology of the SARS-CoV-2 virus justified the rapid action of surgical societies in releasing recommendations based mainly on theoretical considerations. It is now imperative to conduct investigations which produce evidence to guide us in either adjusting past recommendations or to develop new ones. To accurately determine the risk of SARS-CoV-2 transmission during surgery, and in particular during MIS procedures, a careful and scientifically sound evaluation of the presence of the virus in surgical smoke contained in the CO 2 dispersed in the OR should be performed. Very often some of the measures called out to reduce the risk of potential viral exposure to the OR team were issued without considering a patients' health or the impact a recommendation would have on surgical outcomes. The recommendations included several regions covering the globe and in general did not differ across the globe. The recommendations were generally simple to implement; the only recommendation a region may have difficulty addressing for financial reasons is using a smoke evacuator during electrosurgery.
Unfortunately, compliance with recommendation is always an issue and even the strongest, data-based recommendations regarding behavior need to be fully implemented to be effective. The best practices model continues to evolve as literature concerning the coronavirus develops. The surgical staff needs to keep abreast of the latest literature concerning the safety measures to be taken during surgical procedures.
The COVID-19 has been a burden since the beginning of 2020, and notwithstanding the ongoing vaccination strategy, it is believed the SARS-CoV-2 virus will not disappear quickly. No health care system can withstand the restrictive measures which were adopted in the first phase of the pandemic, such as suspending elective surgeries and surgical consultations. Protocols and practical measures should be implemented to sustain a safe surgical environment for both the OR teams and their patients. The development, release and implementation of evidence-based recommendations and guidelines should be the foundation during this and future pandemics to ensure the health care system provides the best surgical and medical care globally.