Abstract
Background. Laparoscopic surgery generates end products that can have potentially harmful effects for the surgical team from short- or long-time exposure. In view of the current SARS-CoV-2 circumstances, controversy has risen concerning the safety of surgical smoke (SS) and aerosols and the perception of an increased risk of exposure during laparoscopic surgery. Methods. The present qualitative systematic review was conducted according to Meta-Analyses and Systematic Reviews of Observational Studies (MOOSE). A literature search was performed from March 2020 up to May 10, 2020, using the PubMed database, Cochrane, and Google Scholar to assess the risk of airborne transmission of viruses and the potential health risk of surgical smoke- and aerosol-generating procedures produced during laparoscopic surgery. The keywords were introduced in combination to obtain better search results. Application of the inclusion and exclusion criteria identified 44 relevant articles. Results. Genetic material from certain viruses, or the virus itself, has been detected in SS and aerosols. However, in the current SARS-CoV-2, as in other coronavirus situations, studies analyzing the presence of airborne transmission of viruses in surgical smoke are lacking. Conclusion. Despite the lack of clear evidence regarding the risk of diseases as the result of smoke- and aerosol-generating procedures during laparoscopic surgery, further investigation is needed. Meanwhile, all available precautions must be taken.
Keywords
Introduction
Laparoscopic surgery is currently a standard of care for the management of many surgical diseases. However, not all technology-related problems, such as surgical smoke (SS) evacuation, have been solved. The potential health risk arising from the smoke emitted during laser surgery, laparoscopic surgery, and electrocautery is a constant problem that is not well understood or studied. 1
In the present COVID-19 pandemic, there is concern among surgeons regarding the potential risk of viral transmission through the smoke or aerosols originated by electrocautery or energy devices (ultrasonic shears) during laparoscopic surgery. 2 Despite the recommendations of surgical associations and specialists in laparoscopy, such possibilities have not been ruled out, and COVID-19 RNA has been detected throughout the respiratory tract, in feces, in the intestinal mucosa, and in peritoneal fluid.3,4
In this framework, the management of surgical patients has been greatly affected and approaches will change in a more or less permanent way. Studies to prepare for possible bioterrorist attacks have been revived, leading to concern about the potential for the transmission of airborne agents such as influenza, severe acute respiratory syndrome-associated coronaviruses (2003) (SARS-CoV), influenza virus (2009) (A H1N1P), 5 Middle East respiratory syndrome (2012, MERS), and the recently emerged coronavirus “(COVID-19).”
With the appearance of viruses such as COVID-19 or other new pandemic risk situations, surgeons need to be aware of the potential risks of SS in the practice of surgery. The rationale is that if the genome of the organism is present in the air, it is reasonable to assume that the viable organism may also be present. In this case, it could potentially be inhaled by a susceptible host.
Our aim was to analyze the existing evidence in the literature regarding the risk that exposure to smoke and aerosols generated during laparoscopy surgery entails for surgeons.
Methods
Search Strategy
We conducted a qualitative systematic review in accordance with Meta-Analyses and Systematic Reviews of Observational Studies (MOOSE). The search used 3 search domains of medical subject heading (MeSH) terms combined by ‘‘AND’’: 1. “Surgical Smoke,” 2 “Laparoscopy,” and 3 “Airborne transmission.” Within each domain, the terms were combined with ‘‘OR’’:1 “Viral transmission”; 2- “COVID-19”; 3 “Operating Room prevention.” No language restrictions were applied. Eligibility assessment was performed independently in an unblinded standardized manner by 2 reviewers. Disagreements were resolved by consensus. The last search date was May 14, 2020.
Inclusion and exclusion criteria
All abstracts of articles resulted from the search were screened. Articles in English relevant to our focus were selected. Only original articles were included. Our eligibility criteria were based on studies and publications that involved the potential risk of aerosols produced by laparoscopy to transmit viral diseases. They included the constituents found in SS, the implications of exposure to smoke, and the type of energy-based surgical instrument that generated the smoke.
Studies were excluded if they were preclinical experimental work, conference abstracts, opinion-based reports, duplicate articles, or incomplete studies.
Data Extraction, Outcome Measures, and Analysis
The following sources were searched for studies concerning the evaluation of SS and its disease transmission capacity: PubMed (2800), Cochrane, 44 and Google Scholar (8110). The search was performed by 3 investigators independently. Reviewers were blinded to studies selected for inclusion by the other reviewer. Discrepancies were resolved by a third party. Bibliographic references of published studies and reviews were also interrogated. Data were extracted using a standardized data collection form.
The authors read and evaluated each of the articles selected. All sources are cited where appropriate (Figure 1). Results of the search technique.
Methodological Quality of Included Studies
All studies were assessed for methodological quality using the Newcastle-Ottawa Scale (NOS). This scale evaluates the methodology quality in 3 domains, patient selection, comparability, and outcome, with the maximum grade being 9 points. Studies with a score of 8 or higher were classified as high quality, 4 to 8 as moderate, and less than 4 as low. To evaluate the randomized control trial, we used the revised tool to assess the risk of bias in randomized trials (ROB 2.0). IRB approval and written consent were not required for this study.
Results
Study Selection and Quality Assessment
The searches of the electronic databases retrieved 10 954 records. Reviewers excluded duplicates, titles, and abstracts after screening. From these, 108 articles were selected for full-text review. A second review permitted to reject nonhuman related papers (n:64). Forty-four articles fulfilled the eligibility criteria and were finally included in the qualitative analysis. All articles were classified according to the area covered.
Study Characteristics
All articles included were published from 1980 to May 10, 2020, and all were written in English. They were all original articles covering the search areas. Of the 44 articles reviewed, 17 were nonrandomized comparative trials, 14 were descriptive research articles, 7 were systematic reviews, 4 were expert opinion, 1 was a guideline, and 1 was a randomized control trial.
Quality Assessment Scale (Newcastle-Ottawa).

Studies reviewed.
Data Synthesis
Aerosolized particles during surgery
Chemicals in laparoscopy
Carcinogen B1 = animal bioassay, but not sufficient human evidence.
Carcinogen A = known human carcinogen.
Surgical Smoke Viable Microorganism
Hepatitis B virus
We found only one article that evaluated the SS produced in laparoscopy (Table 5). In this study, 11 patients, all positive for hepatitis B surface antigen (HBsAg), underwent different gastrointestinal surgeries by laparoscopy or robotic surgery. The authors collected and analyzed this smoke using PCR and demonstrated detectable Hepatitis B Virus (HBV) in 10 of 11 cases. 19 However, the infectivity of this surgical plume was not evaluated.
Aerosolized human papilloma virus DNA
Human immunodeficiency virus
In one study that analyzed the SS generated by electrocautery used in blood samples containing HIV-1, smoke was suctioned through the culture medium, but no infectious Human Immunodeficiency Virus (HIV)-1 was detected. 23 Baggish et al studied the SS produced from CO2 laser by vaporizing a sample of 10 mL HIV-infected cells. They identified the presence of HIV p24 protein for at least 14 days in one case, and the cultured cells were also PCR positive for proviral DNA. 24
Emerging coronaviruses: Severe acute respiratory syndrome, middle east respiratory syndrome, and severe acute respiratory syndrome coronavirus
Coronaviruses are lipid-enveloped, single-stranded positive sense RNA viruses and include 3 virulent coronaviruses: severe acute respiratory syndrome coronavirus (SARS-CoV), which emerged in the human population in 2003; Middle East respiratory syndrome coronavirus (MERS-CoV), which emerged in humans during 2012; and SARS-CoV-2, which emerged in 2019. 25
Tran et al analyzed 4 case control studies and concluded that tracheal intubation was a significant risk factor for transmission of SARS to HCWs. A summary estimate (using a random effects model) for the case-control studies yielded an OR of 6.6 (95% CI 4.1, 10.6) with high statistical heterogeneity (I2 = 61.4%). 26
Other aerosol-generating procedures with an increased risk of transmission for SARS among HCWs were noninvasive ventilation, tracheotomy, and manual ventilation before intubation. 29 We did not find any studies evaluating exposure to SS as a risk factor for the transmission of these viruses.
SARS-CoV-2
What we know so far regarding SARS-CoV-2 is that the RNA virus has a size range of .06 to .14 μm, and it has been detected in specimens from multiple sites of patients with COVID-19. 27 One study showed that samples most commonly test positive for the virus in the lower respiratory tract. Bronchoalveolar lavage fluid specimens showed 93% of positive rates, nasal swabs 63%, fibrobronchoscopy brush biopsy 46%, and pharyngeal swabs 32%. The live virus was also detected in feces (29%) and blood (1%).
In Singapore, it was reported that 17% of patients with COVID-19 reported diarrhea, and SARS-CoV-2 was detected in stool samples from 50% patients, but it was not clearly associated with abdominal symptoms.28-30 Coccolini et al reported a patient with SARS-CoV-2 pneumonia who underwent surgery for small bowel volvulus. During the surgery, 2 samples of peritoneal fluid were found to be positive, and the viral load in the peritoneal fluid was higher than that in upper respiratory material. 31
Neeltje et al reported that SARS-CoV-2 remained viable in aerosols throughout their experiment (3 hours), with a reduction in infectious titer from 103.5 to 102.7 TCID50 per liter of air. The longest viability was on stainless steel and plastic; the estimated median half-life of SARS-CoV-2 was approximately 5.6 hours on stainless steel and 6.8 hours on plastic. The authors concluded that aerosol and fomite transmission of SARS-CoV-2 is plausible since the virus can remain viable and infectious in aerosols for hours and on surfaces for days. However, this study did not evaluate the SS. 32
Infection risk
Concerning SS infectivity, we found only 2 studies that evaluated this. The first was an in vitro study where SS produced by YAG laser tested positive for retrovirus. When exposed to different cells, it showed that viruses contained in laser vapors remained infectious and capable of integrating into the genome of susceptible cells. 33 In another article, conducted in animals, bovine papillomavirus-induced cutaneous fibropapillomas were exposed to CO2 laser. The laser aerosol was then suctioned and reinoculated onto the skin of calves. All the samples contained substantial amounts of BPV DNA. The sites that were inoculated with the SS samples developed tumors, and histological and biochemical studies revealed that these tumors were infected by the same virus as that present in the laser smoke. 34
Prevention
Personal protection
Studies Investigating the Filtration Efficiency of Masks. 43
Barret et al reported that HEPA masks such as the N95 respirator should be considered when possible, though surgical masks can filter most noxious chemicals generated in SS and should be worn whenever possible. 12 Mandatory compliance with smoke evacuation must be ensured in all operating rooms to maintain a healthy environment for the surgical team. Operating rooms must have a minimum of 15-20 air changes per hour and the pressure within them must be positive with respect to that of their environment. However, this is not enough to treat the smoke created during laparoscopy, and other measures, such as the use of personal protective equipment, vacuum cleaners, and aspiration systems, should be combined. 38
Innovations in technology to improve air quality in the operating room have been introduced. These include controls that maintain a positive air pressure in relation to nearby areas and regulate the speed of replacement. They control temperature and humidity as well as air filtration in the operating room. 39
Commercially Available Smoke Evacuation Systems. 44
*Reproduced from a document published by the Society of Gastrointestinal and Endoscopic Surgeons in conjunction with their guidelines for surgeons concerning the use of laparoscopy during the current COVID-19 pandemic.
Discussion
We found a great variety of studies and methodological designs that suggest a risk or possibility of viral transmission through SS. Smoke samples were collected and analyzed in different ways, resulting in differences in the concentrations of the isolated components and in the size of the studied particles. Since these studies differ in terms of methodology and characteristics, it is difficult to compare them.
Besides the hazardous products that SS can carry and the harmful effect that they can have on healthcare personnel, the infectious capacity of this smoke is also of concern. Several studies have isolated viruses such as HPV, HBV, HIV, and also some bacteria.19-24,33,34 However, to date, none of the studies carried out on humans have assessed or demonstrated the ability of this smoke to transmit an infection caused by the microorganism it carries.
On the other hand, one in vitro study showed that some retroviruses present in SS were able to integrate into the genome of susceptible cells, and another study showed that the bovine papillomavirus present in CO2 laser smoke was able to induce tumors on the skin of the animal where it was inoculated,33,34 making it likely that SS is capable of generating an infection in HCWs.
It has been demonstrated that new coronavirus, SARS-CoV-2, can be transmitted by aerosols, as well as by direct contact or indirect contact by fomites. Its RNA has been identified in the respiratory tract, blood, feces, and, more recently, in peritoneal fluid, but as yet there is little evidence related to the relative risk of health personnel involved in laparoscopic surgery or open surgery on patients with COVID-19.
Although the transmission of biological material has been demonstrated, the risk of transmission is low. Nevertheless, prudence recommends the implementation of preventive measures such as those suggested by SAGES on how to reduce the possibility of transmission through aerosols in the operating room when using laparoscopy. Aerosol-generating procedures can contain viruses, and in some cases, they have led to infection. However, to date, no data have demonstrated the presence of SARS-CoV-2 in the smoke generated during a surgical procedure. In fact, non-respiratory transmission is still under investigation. On the other hand, fecal-oral transmission has also been suggested, while viral clearance modality and its timing are not entirely understood. 41
Concern about the risk of infection associated with the use of laparoscopy has risen. In fact, data shown in this analysis highlights the risk that SS generated during laparoscopy could transmit to the surgical team. Colorectal surgery is an especially worrisome situation. Of particular concern is the opening of the colon lumen for a colonic resection and its preparation for the anastomosis when endoluminal gas is released. Another hypothetically risky situation occurs during TATME or TEM procedures, in which a pneumorectum is induced and needs to be deflated.30,33 As a result, several authors have suggested reducing working pressure during abdominal laparoscopy to a minimum, and others have questioned whether laparoscopy should be used at all during pandemics.
Standard electrostatic filters used for ventilation machines have the capability of filtering known bacterial and viral loads with great efficiency and effective protection against HBV that have a diameter of 42 nm. This characteristic of the filters used would be good enough to protect from SARS-CoV-2 which has a larger diameter (70-90 nm). Therefore, the same filtering efficiency can be expected to apply for new virus.
The Royal College of Surgeons of Edinburgh published specific guidelines for surgical care to protect patients and surgeons, but based on the evidence gathered to date, we disagree with the statement that laparoscopy should be avoided. A safe and reliable filtering and evacuation system for pneumoperitoneum gases is used in laparoscopy, making it potentially preferable to open surgery where smoke evacuation and contamination is ungovernable. 42
The SARS-CoV-2 pandemic hit us hard and showed we were prepared for a worldwide emergency. We have learned on the go. We believe that good things can emerge from this tragedy, including better protection for HCWs in the operating room area. However, deeper study into the infectious capacity of SS is recommended.
Conclusions
We did not find any definitive scientific evidence on the transmission of COVID-19 in the SS created by laparoscopy. Despite the lack of clear evidence regarding the risk of disease transmission by aerosols used in laparoscopic procedures, we must take all available precautions. The best practice to stop possible infectious transmission is to use a multifaceted approach that includes an adequate filtration and ventilation system in the OR, assure appropriate protective equipment for all the HCWs in OR, and install smoke evacuators with suction and filtration systems.
Recommendations
There is no consensus regarding what should be done about SS. Further experimental and epidemiological evidence is required for better assessment of risk prevention, so in meantime, the surgical team must take all necessary measures to protect themselves and prevent the spread of disease. The use of ESTs should be decreased as much as possible during laparoscopy. Smoke evacuation devices with high-efficiency particulate air (HEPA) filters should be used.
Footnotes
Author Contributions
Study concept and design: Jorge Pasquier, Sunaymy Sarria Lamorú, and Oscar Villalta
Acquisition of data: Jorge Pasquier, Sunaymy Sarria Lamorú, and Oscar Villalta
Analysis and interpretation: Jorge Pasquier, Sunaymy Sarria Lamorú, and Oscar Villalta
Study supervision: Ramon Vilallonga, Carmen Balagué, and Eduardo M. Targarona
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
