COVID-19 and Laparoscopic Surgery: Scoping Review of Current Literature and Local Expertise

Background: The current coronavirus disease (COVID-19) pandemic is holding the world in its grip. Epidemiologists have shown that the mortality risks are higher when the health care system is subjected to pressure from COVID-19. It is therefore of great importance to maintain the health of health care providers and prevent contamination. An important group who will be required to treat patients with COVID-19


Introduction Background
Coronavirus disease (COVID-19) is spreading worldwide, and all health care workers are affected by it [1]. At the moment of writing, the World Health Organization estimated over 2.5 million confirmed cases of COVID-19 and over 175 thousand deaths [2]. It is estimated from the Chinese outbreak that the risk of death is as high as 12% in epicenters of the epidemic and as low as 1% in less severely affected areas. This large difference may be due to a breakdown of the health care system in the epicenter, enhanced public health interventions, and enhanced hygienic measures [3].
According to Médecins Sans Frontières, nearly 1700 healthcare providers have been infected, representing 8% of the total COVID-19 cases in Italy, despite all preventive measures [4]. Therefore, health care providers are the highest risk group for infection, severe illness, and intensive care admission. This stresses the incredible importance of protecting this group.
Due to the combination of increased risk of individual infection and the effects of a breakdown of the healthcare system, it is even more relevant to discuss how to properly protect health care providers. If no personal protective equipment is available, health care workers will be jeopardized [5,6]. Moreover, the shortage of supplies is forcing management to make difficult decisions as to where supplies should be allocated and who needs them most in a hospital.
So, who is at risk? According to the US Centers for Disease Control and Prevention, all health care providers that are in direct contact with infectious secretions from a patient with COVID-19 are at risk. Secretions at risk for viral transmission include sputum, serum, blood, feces, and especially respiratory droplets [7,8]. Health care providers are all recommended to wear personal protective equipment (PPE). The risk increases with exposure to aerosol-generating procedures for at least 10 minutes at a distance of fewer than 2 meters from the patient [9]. Studies have shown that procedures such as endotracheal intubation, extubation, noninvasive ventilation, and exposure to aerosols in an open circuit are associated with high risk of viral transmission. Guidelines about the PPE needed in these situations are receiving increasing attention [10].
According to Wong et al [11], the main risk groups in the operating theater are those who cannot cancel or delay elective procedures. Foremost, of course, are anesthesiologists; however, departments such as intervention radiology, obstetrics, and cardiothoracic surgery are also at risk. Many acute surgical interventions are performed by laparoscopy; however, very little is written about the risks for health care providers of performing laparoscopic surgery on a patient with COVID-19. There is a debate in the literature whether open surgery is safer for health care providers compared to laparoscopic surgery [12,13].
The objective of this study is to provide an overview of potential contamination routes and possible risks for health care providers, and propose research questions based on current literature and expert opinions about laparoscopic surgery on patients with COVID-19.

Theoretical Contamination Routes During Laparoscopic Surgery
Before we can elaborate on the theoretical contamination routes, we must first discuss the contamination agents. The agents of contamination can be divided into three groups: those with proven infectious transmission, such as droplets, close contact, and aerosol transmission [14]; those with proven RNA presence, but no proven contamination yet, such as feces, inanimate surfaces, and blood [8,15,16]; and unknown or highly debated agents or even the presence of RNA, such as urine and amniotic fluid [8]. It should be noted that many studies are underway to determine which of these agents are, in addition to containing virus RNA, are also infectious. Taking these agents into consideration, there are several theoretical contamination routes by which health care providers can be infected by a COVID-19 positive patient. Figure 1 shows potential viral contamination routes in the IR during laparoscopic surgery. The first and most discussed contamination route is intubation and extubation [17]. At this moment, the patient will excrete the most virulent respiratory secretions. The second risk is smoke and air evacuation during surgery [18]. During laparoscopy, smoke and aerosols are generated, not only by cauterization of blood vessels but also by dissection. This smoke can contain virulent DNA and RNA and is sometimes evacuated directly into the overpressured operating room (OR) by opening a valve on a trocar. The third contamination risk is tissue extraction [19]. Removing tissue, such as an appendix, bowel segment, gallbladder, cyst, or ectopic pregnancy, can cause excretions to be expelled from the body; the higher abdominal pressure from laparoscopy creates aerosols from excretions such as blood and mucus. The fourth moment at risk for contamination is at the end of the surgery, when the abdominal pressure is released by desufflation [19]. All the air, possibly filled with virulent DNA and RNA, is released into the air of the OR, usually under relatively high pressure. A fifth risk factor can be the positive air pressure in the OR, which pushes aerosols out of the OR into hallways and other ORs [17].

Methods
To provide insight into the possible risks of the abovementioned contaminating routes, we believe a scoping review is most suited. A scoping review allows a broader search and answers multiple questions while still performing a systematic search [20]. Because we expected few results from a search on COVID-19 and laparoscopy, we performed five additional searches for the contamination route and viruses in general.

Systematic Search
The literature search was performed on April 24, 2020, by searching the PubMed, CINAHL, and Embase databases. We then added gray literature from Google Scholar and local expertise and handbooks from the authors themselves from China, Italy, Spain, the United Kingdom, and the Netherlands. The search string can be found in Multimedia Appendix 1. The five additional questions were: 1. What is the effect of operating room pressure on the contamination risk of COVID-19? 2. What is known about the additional risk during intubation and extubation? 3. Does smoke evacuation during laparoscopic surgery increase the risk of the spread of COVID-19 particles? 4. Is anything known about tissue extraction during laparoscopic surgery on a patient with COVID-19? 5. Does desufflation of the abdomen after laparoscopic surgery create airborne aerosols that endanger health care providers?

Inclusion Criteria
Types of studies included were trials, reviews, case studies or series, and other descriptive studies concerning contamination of health care providers during (laparoscopic) surgery in the operating theater. We also included expert opinions if they added additional insight to the current literature.

Exclusion Criteria
We excluded society and professional association statements about COVID-19 if they did not add any new information. We did use them to snowball their references. We also excluded commentaries such as letters to the editor and papers not written in English.

Study Selection
Working independently and in duplicate, reviewers RDL and NB screened all record titles and abstracts. Potentially eligible abstracts and abstracts with disagreement or insufficient information were screened in full text. Disagreements were addressed by discussion of the full text. Papers were excluded because they discussed a treatment therapy or diagnostic method (118/267, 44.2%), did not provide any new information (society statements, letters to the editor and others) (30/267, 11.2%), were not related to our question (12/267, 4.5%) or were not available in English (9/267, 3.4%).

Literature Search
After hand-searching the papers and society statements, we were left with 60 papers for this review. Of these 60 papers, 21 (35%) concerned COVID-19, and 39 (65%) discussed our questions in regard to other viral transmissions. We will now discuss the results for each of the five proposed questions.

What is the Effect of Operating Room Pressure on the Contamination Risk of COVID-19?
We found 8 papers discussing the effects of OR safety and the spread of virus DNA. Only 1 paper actually discussed the experience with COVID-19 in Wuhan [11], and all studies were based on theoretical risks (see Table 1). An OR with a negative pressure environment is ideal to reduce dissemination of the virus by preventing air from escaping the OR [11]. Both the Society of American Gastrointestinal and Endoscopic Surgeons (SAGAS) and the American Society of Gastrointestinal Endoscopy advise that surgery be performed in negative pressure ORs [29,30]. However, a standard OR is usually designed to be at positive pressure relative to the surrounding air. Tien et al [25] reported that during the severe acute respiratory syndrome (SARS) outbreak, surgical procedures were performed within airborne isolation Intensive Care Unit rooms and with additional PPE precautions. This eliminated the risk of intrafacility transport and avoided the need to make environmental modifications to the operating room. Other papers discuss the same contamination route with SARS and Middle Eastern respiratory syndrome (MERS) [22][23][24]26]. Beasley et al [27] discussed even more isolation strategies in the case of surgery on patients with smallpox.
In Singapore, dedicated separate ORs for surgery on patients with COVID-19 have been installed. The aim was to reduce the risk of contamination of other ORs and patients. Each OR had its own ventilation system with an integrated high-efficiency particulate air (HEPA) filter. The traffic and flow of contaminated air were minimized by locking all doors to the OR during surgery, with only one possible route for entry and exit via the scrub room [11].
Wax et al [31] provided practical recommendations to decrease viral spread when managing a patient infected with COVID-19. Their advice is to convert operating rooms to negative pressure environments with airflow changes.

What is Known About the Additional Risk During Intubation and Extubation?
Thirteen papers were found discussing intubation and extubation of patients with COVID-19 (see Table 2). Another 19 papers discuss the risk of intubation for health care providers for viruses other than severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2, Multimedia Appendix 2).  [32] Anesthesia guidelines Review Canada Wax [31] 3/121 (24.8%) of health care professionals tested positive Case series United States Heinzerling [33] 29% of hospitalized COVID-19 b patients were health care providers Experience paper China Meng [34] High level PPE for aerosol-generating procedures Experience paper Italy Sorbello [35] Anesthesia advice for intubation Experience paper China Yao [36] Anesthetic management guidelines Retrospective cohort study China Zhao [21] Anesthesia guidelines Experience paper China Zuo [37] Complete COVID-19 overview Experience paper Italy Giwa [38] Intubation advice Review United States Greenland [39] Anesthesia advice Expert opinion South Korea Kim [40] Intubation advice Experience paper Singapore Au Yong [41] No health care providers infected Case series China Zhang [42] a PPE: personal protective equipment. b COVID-19: coronavirus disease. Two reviews from Cook et al [32] and Wax et al [31] provide a great overview of current knowledge and stress the increased risk to health care providers during intubation and extubation. A case series by van Heinzerling [33] shows that 3/121 health care providers (2.5%) tested positive after assisting intubation.
Zucco at al [43] warn that the anesthesia professionals and intensivists have the highest risk of exposure to respiratory droplets during intubation and extubation. They provide a 10-point list of precautions that should be taken into account when intubating or extubating patients with COVID-19 [44]. Again, Wax et al [31] advise that high-risk aerosol-generating procedures, such as intubation, not be performed in a positive pressure environment. Won et al [11] advise the use of at least a National Institute for Occupational Safety and Health (NIOSH)-certified N95 respirator, eye protection (either goggles or a full face shield), cap, gown, and gloves. As transmission remains possible despite N95 protection, staff participating in aerosol-generating procedures can wear a powered air purifying respirator (PAPR). Repici et al [45] suggest additional PPE during endoscopic procedures but does not provide additional insight into the risks of intubation.
Learning from other experiences, 16 studies stress the increased risk for health care providers during intubation from the 2003 SARS period (Multimedia Appendix 2). Pei et al [22] show that the odds ratio (OR) that a health care provider will be infected is 30.8. While others show lower numbers (Rabout et al [46] 2.79 and Tran et al [47] 6.6), they all label intubation as a very high-risk procedure for health care providers.

Does Smoke Evacuation During Laparoscopic Surgery Increase the Risk of the Spread of COVID-19 Particles?
We found 25 papers discussing the effects of surgical smoke on health care providers. However, none of these papers is specific to COVID-19. A review from Mowbay et al [48] from 2013 included 20 studies and showed the diverse outcomes of these studies; they concluded that infective virus DNA can be found in the smoke plume, but the risk to OR staff is unproven. We found 19 studies not mentioned in the Mowbay review (see Table 3) that also showed diverse results. In Korea, Kwak et al [49] found hepatitis B DNA in surgical smoke in 10/11 cases; however, Waynandt [50] did not find any human papillomavirus (HPV) in 28 cases of CO 2 laser plume. However, another study [51] shows that laparoscopic surgery is associated with better preservation of the immune system than open surgery. This results in a decreased incidence of infectious complications. A systematic review concerning surgical smoke during open surgery [48] shows that in terms of infection risk, 6/20 (30%) of the studies assessed surgical smoke for the presence of viruses, with only 1 study (5%) positively identifying viral DNA in laser-derived smoke. This has been shown for HPV DNA [52,53].

Is Anything Known About Tissue Extraction During Laparoscopic Surgery on a Patient With COVID-19?
We found no studies found concerning this subject. The only studies that we found concerned malignant cells; however, those were out of the scope of this review. One study [70] showed that during laparoscopic surgery, 48.5% of surgeons' masks, 29.5% of assisting surgeons' masks, and 31.8% of scrub nurses' masks were positive for either visible or visually enhanced blood contamination. This demonstrates that wearing masks is of great importance, even when performing laparoscopic surgery.

Does Desufflation of the Abdomen After Laparoscopic Surgery Create Airborne Aerosols That Endanger Health Care Providers?
One case study discussed the desufflation of CO 2 gas used during laparoscopic rectal surgery [71]. SAGES recently stated that there is a good possibility of viral contamination during laparoscopy; they added, "While it is unknown whether coronavirus shares these properties, it has been established that other viruses can be released during laparoscopy with carbon dioxide." However, this has only been shown in smoke, not clear CO 2 [72].
In one study, the effects of COVID-19 on the strategy for colorectal cancer patients is discussed. The authors especially recommend that natural orifice specimen extraction surgery and transanal total mesorectal excision should be performed with caution during the epidemic period because fecal-oral transmission and aerosol transmission during this type of surgery have not been excluded. A protective stoma should reasonably be carried out, and the protection of OR personnel should be strengthened [73].

Discussion
There is some existential consensus in the literature that intubation and extubation are high-risk procedures for health care providers. Studies have shown ORs as high as 30, stressing the importance of proper PPE during those procedures [22]. Literature suggests that intubation and extubation should preferably be performed in a low-pressure environment with protective gear for the health care providers. A reasonable number of studies show that surgical smoke contains viral DNA JMIR Public Health Surveill 2020 | vol. 6 | iss. 2 | e18928 | p. 7 http://publichealth.jmir.org/2020/2/e18928/ (page number not for citation purposes) de Leeuw et al JMIR PUBLIC HEALTH AND SURVEILLANCE

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RenderX and that health care providers should avoid inhaling it. The infectiousness of tissue extraction and the insufflation gas itself is absolutely unknown, and all advice is at least "arguable" (see Table 4).
When current knowledge does not help us any further, we are faced with a dilemma. Should we follow the conservative route and provide extensive PPE and prevent surgery at all costs? This may sound like the safe option; however, performing surgery wearing a PAPR [11] may not even be possible. In addition, delaying surgery may cause a patient more harm due to disease progression. Also, as COVID-19 continues to spread, resources are getting low, and it might not be possible to provide each health care provider with proper PPE. In that case, we should start to distribute resources where they are needed most, but also where the evidence provides insight into their effectiveness.  [74], has not been peer-reviewed and published in the literature; however, it does provide important lessons from previous outbreaks. The authors consider any kind of surgery to be high risk and advise level III protection during surgery (ie, surgical cap, N95 protective mask, work uniform, disposable medical protective uniform, disposable latex gloves, and a full-face PAPR device), negative pressure operating rooms and several other hygiene precautions [74].
Textbox 1 provides a summary of our recommendations. • Postpone elective surgery.
• Consider screening every patient who needs emergency surgery for COVID-19 either by PCR swab or CT scan of the thorax.
• Dedicate specific operating rooms to patients with COVID-19.
• Turn off positive pressure/create negative pressure ORs.
• Use Level III personal protective equipment during intubation and extubation.
• Consider Level III PPE but at least provide adequate mouth, face, and eye protection during surgery.
• Use proper filters and closed systems for smoke evacuation.
• Use proper filters and closed systems for CO 2 desufflation.
• Do not perform transanal surgery.
• Consider faces as contaminated fluids.

Preventive Measures
All studies emphasize the importance of protecting health care providers with adequate PPE whether they are performing surgery or a physical examination. However, there are diverse interpretations of how to use PPE. There are many studies examining, for example, face masks [77][78][79]. The debate is focused on the added value of giving the patient a mask [78] or which mask to use [79,80]. Some studies provide hospital-made protective gear solutions in case of limited resources [81] or show the added value of salt-covered masks [82]. Finally, studies that show the influence of transocular infection of influence advise the use of N95 protective gear for the eyes as well [83].
Focusing on other contamination routes, Hahn et al [84] showed that a built-in-filter trocar removes >60% of hazardous molecules during laparoscopic rectal resection, and companies are registering these trocars. SAGAS and others advise that the use of devices to filter aerosolized particles in released CO 2 should be strongly considered and that the high pressure in the OR should be turned off or, even better, low pressure ORs should be created. A few dedicated ORs should be created for the purpose of performing emergency surgery on patients who have or are at high risk for COVID-19.
Health care providers should think logically about tissue extraction, protect themselves and OR staff, desufflate the abdomen first, and not hesitate to increase the incision slightly rather than increasing the risk of the spread of aerosols. Finally, when desufflating, use of a filter should be considered or the same system as the smoke evacuation should be used.

Conclusions
To conclude, we would like to look forward. There is ongoing debate on the preoperative screening of asymptomatic patients and how to proceed when the peak of the crisis is over and elective surgeries can be performed again. To screen patients who are asymptomatic for COVID-19, earlier SARS-CoV-2 outbreak studies show higher sensitivity of computerized tomography (CT) scanning compared to polymerase chain reaction (PCR) swabbing [85,86]. However, more recent studies debate the actual added value in absolute numbers and the risks of false-positive outcomes even when using new classification systems [87,88]. Future studies are needed to provide proper advice about COVID-19 screening. Most of all, health care providers should use logic and common sense to protect themselves and others by performing surgery in a safe and protected environment. A global effort is being made to report on the experience and outcomes of surgical patients with COVID-19. The study protocol, registration, and details can be found at the website [89].

Authors' Contributions
The search was performed by RAdL and JH. Additional papers were added by JT, JZ, and PA. Local expertise was provided by MM, PB, JB, and MC. All authors read and approved the final manuscript.

Conflicts of Interest
None declared.

Multimedia Appendix 1
Search string.