key: cord-0309925-gwo0g5ii
authors: Lee, P.; Kozak, R.; Alavi, N.; Mbareche, H.; Kung, R.; Murphy, K.; Perruzza, D.; Jarvi, S.; Salvant, E.; Ladhani, N. N.; Yee, A.; Gagnon, L.-H.; Jenkinson, R.; Liu, G. Y.
title: Detection of SARS CoV-2 contamination in the Operating Room and Birthing Room Setting: Risks to attending health care workers
date: 2021-09-07
journal: nan
DOI: 10.1101/2021.09.03.21262874
sha: 25fd6d6f3f7e50b4a59882a29e47bec4ff5943a1
doc_id: 309925
cord_uid: gwo0g5ii

Background: The exposure risks to front-line health care workers who are in close proximity for prolonged periods of time, caring for COVID-19 patients undergoing surgery or obstetrical delivery is unclear. Understanding of sample types that may harbour virus is important for evaluating risk. Objectives To determine if SARS-CoV-2 viral RNA from patients with COVID-19 undergoing surgery or obstetrical care is present in: 1) the peritoneal cavity of males and females 2) the female reproductive tract, 3) the environment of the surgery or delivery suite (surgical instruments, equipment used, air or floors) and 4) inside the masks of the attending health care workers. Methods The presence of SARS-CoV-2 viral RNA in patient, environmental and air samples was identified by real time reverse transcriptase polymerase chain reaction (RT-PCR). Air samples were collected using both active and passive sampling techniques. Results In this multi-centre observational case series, 32 patients with COVID-19 underwent urgent surgery or obstetrical delivery and 332 patient and environmental samples were collected and analyzed to determine if SARS-CoV-2 RNA was present. SARS-CoV-2 RNA was detected in: 4/24(16.7%) patient samples, 5/60(8.3%) floor, 1/54(1.9%) air, 10/23(43.5%) surgical instruments/equipment, 0/24 cautery filters and 0/143 inner surface of mask samples. Conclusions While there is evidence of SARS-CoV-2 RNA in the surgical and obstetrical operative environment (6% of samples taken), the finding of no detectable virus inside the masks worn by the medical teams would suggest a low risk of infection for our health care workers using appropriate personal protective equipment (PPE).

The exposure risks to front-line health care workers who are in close proximity for prolonged periods of time, caring for COVID-19 patients undergoing surgery or obstetrical delivery is unclear. Understanding of sample types that may harbour virus is important for evaluating risk.

To determine if SARS-CoV-2 viral RNA from patients with COVID-19 undergoing surgery or obstetrical care is present in: 1) the peritoneal cavity of males and females 2) the female reproductive tract, 3) the environment of the surgery or delivery suite (surgical instruments, equipment used, air or floors) and 4) inside the masks of the attending health care workers.

The presence of SARS-CoV-2 viral RNA in patient, environmental and air samples was identified by real time reverse transcriptase polymerase chain reaction (RT-PCR). Air samples were collected using both active and passive sampling techniques.

In this multi-centre observational case series, 32 patients with COVID-19 underwent urgent surgery or obstetrical delivery and 332 patient and environmental samples were collected and analyzed to determine if SARS-CoV-2 RNA was present. SARS-CoV-2 RNA was detected in: 4/24(16.7%) patient samples, 5/60(8.3%) floor, 1/54(1.9%) air, 10/23(43.5%) surgical instruments/equipment, 0/24 cautery filters and 0/143 inner surface of mask samples.

While there is evidence of SARS-CoV-2 RNA in the surgical and obstetrical operative environment (6% of samples taken), the finding of no detectable virus inside the masks worn by the medical teams would suggest a low risk of infection for our health care workers using appropriate personal protective equipment (PPE).

Front line health care providers are at risk of contracting infections when caring for patients with COVID-19 [1] [2] [3] . Moreover, close, direct and often prolonged patient contact is essential in surgery and obstetrics.

However, this may facilitate SARS-CoV-2 infections through the known vectors of respiratory droplets, aerosols and fomites, but infections may potentially be transmitted through exposure to the virus from the surgery or obstetrical delivery itself [4] [5] [6] . It remains unclear if the type of surgical/obstetrical procedure, may present different risks to HCWs attending these patients.

SARS-CoV-2, the virus that causes COVID-19 can spread via respiratory droplets and aerosols of infected persons through coughing, sneezing or talking [7] [8] [9] [10] . Additionally, the virus has been documented to be present in the gastrointestinal (GI) tract and consequently any surgery that involves opening the GI tract (bowel related surgery) is thought to pose a risk to medical teams 11, 12 . There are case reports of SARS-CoV-2 virus detected in peritoneal fluid from a patient with COVID-19 undergoing surgery 13, 14 . In the female reproductive tract, SARS-CoV-2 RNA has been identified in amniotic fluid, vaginal swabbing and documented cases of vertical transmission have been found [15] [16] [17] [18] . Potentially, if the virus is present on peritoneal surfaces of males or females, in the female reproductive tract or the myometrium, this virus could be aerosolized via cautery smoke, or, from the release of CO2 gas from laparoscopic procedures.

While there is no current published research on the presence of SARS-CoV-2 in the surgical smoke/ plume, there is existing literature which identified other viruses including human papillomavirus (HPV), Human Immunodeficiency Virus -1 and Hepatitis B virus in surgical smoke [19] [20] [21] [22] [23] [24] [25] [26] [27] [28] .

The risks of aerosolization from the respiratory tract is recognized 29 , but the risk of SARS-CoV-2 residing in the surgical site and the subsequent risk of aerosolizing this virus from the surgical site is not well studied. SARS-CoV-2 has been found in air samples with research demonstrating that the virus contained in aerosol particles can remain viable in the air for extended periods of time and are potentially infectious after both human shedding and airborne transport 30, 31 . There is documentation of SARS-CoV-2 virus in the hospital ward setting 6, [32] [33] [34] , in the delivery suite 35 and with tracheostomies (an aerosol generating medical procedure) 29 .

. CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review)

The copyright holder for this preprint this version posted September 7, 2021. ; https://doi.org/10.1101/2021.09.03.21262874 doi: medRxiv preprint More importantly, reports on the risks of SARS-CoV-2 viral contamination of the HCW in the operating room (OR) and birthing room setting (apart from studies on tracheostomies) were not identified by this author; although there have been studies reporting on HCW mask viral contamination in the patient ward setting [36] [37] [38] [39] . Since a respiratory route is considered the main route of infection, knowledge of the risks of contamination of the masks is critical to assess the potential risks of viral exposure to the HCW working in the OR/delivery suites.

As COVID-19 is likely to continue to circulate and be endemic, even in the presence of vaccines, knowledge of risks will be essential to determine the optimal means to protect HCWs.

We seek to study the risk of contamination in the OR and birthing suite environment via evaluating the risk of aerosolization from the respiratory tract or from the surgical/obstetrical field during surgery or labor and delivery. This information is key to assessing the risks to HCWs who care for patients at the time of 1) vaginal delivery or cesarean section and 2) other surgical procedures whether they are vaginal, abdominal or laparoscopic. This knowledge would help guide best practice regarding the use of personal protective equipment (PPEs) and safety in the OR and birthing room.

The objectives of this study are to determine if SARS-CoV-2 viral RNA from patients with COVID-19 undergoing surgery or obstetrical care is present in: 1) the peritoneal cavity (males/females), 2) female reproductive tract, 3) on surgical instruments/equipment used, 4) the floor of the procedure rooms, 5) bioaerosols produced during surgery or obstetrical delivery, and 6) inside surgical masks of the attending health care workers.

. CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. HCWs included any consenting HCW present in the operating/delivery room, caring for the patient.

. CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted September 7, 2021. Swabbed samples were collected with either a sterile flocked swab or sterile dental pledget that was pre-moistened with universal transport media (UTM) and immediately placed in 3cc of UTM.

Bioaerosol sampling was obtained via two previously described methods: 1) Active air sampling via the GilAir Plus sampler was used at two locations: as close to the surgical site as possible (within 0.5-1 metres) and 2-3 metres away (Sensidyne®, https://www.sensidyne.com/air-sampling-equipment/gilianair-sampling-pumps/gilair-plus/ ) 42 . Samples were collected with a 37 mm three-piece cassette with 0·8 μm polycarbonate filter, sampling at a rate of 3.5L/min for the duration of the procedure with PCR detection after elution from the filter 2) Passive air sampling was considered in the last 10 cases and involved an open Petri dish to collect any viral particles settling by gravity in the dish (within 1-2 metres of the patient) 34, 35, 40, 43, 44 .

Laboratory Methods:

All collected samples were processed at the Shared Hospital Laboratory (Sunnybrook). Aside from the cautery and active air sample filters, the lab staff were blinded to the source of the sample.

. CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted September 7, 2021. ; https://doi.org/10.1101/2021.09.03.21262874 doi: medRxiv preprint Virus detection was performed by real-time RT-PCR using a multi-target assay currently utilized in the laboratory for detection of the virus 45 .

Additionally, the Ct (cycle threshold) value of the assay as an estimate of the viral load was used and where possible was obtained from the initial diagnostic swab of the patient.

The outcome of interest was SARS-CoV-2 RNA PCR positive samples. Whole genome sequencing was not performed with our surgical/obstetrical samples, but was performed on diagnostic nasopharyngeal swabs when possible, in order to identify variants of concern (VOC).

Sample Size: The primary outcome was the rate of SARS-CoV-2 RNA PCR positive samples from the HCWs masks. The expected outcome was 0% positivity. We planned to study 40 patients with an 

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The copyright holder for this preprint this version posted September 7, 2021. ; https://doi.org/10.1101/2021.09.03.21262874 doi: medRxiv preprint

A total of 32 patients with COVID-19 (Table I) (Table II) Variants of concern (VOC) were identified in 10 cases. Of the 10 VOC cases: 9 were the Alpha variant 13.45-35.29). There was no significant difference in Ct values between these two groups (Mann-Whitney U test, p=0.4561). The Ct values of the initial NP swabs were significantly lower (indicating higher viral loads) in those tested who were subsequently found to have any study sample with SARS-. CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted September 7, 2021. 

Several studies have documented potential risks of SARS-CoV-2 infection to HCWs in the clinic or hospital ward settings 1, 6, 29, 46 . To our knowledge, this is the first study evaluating potential exposure risks to HCWs in the operating room with a variety of surgical procedures. The OR is a unique environment as HCWs are in prolonged and very close contact (hands on) with patients. In our study, we detected SARS-CoV-2 RNA in non-respiratory patient samples (peritoneal fluid, vaginal fluid, myometrium, placenta), surgical equipment/instruments (endotracheal tubes, gastroscope, laparotomy surgical clamps & scissors), and the surgical room environment (floor, air); but no contamination of the surgical masks worn by HCWs was detected.

Our study corroborates earlier studies that have shown evidence of virus in the respiratory tract and in some of the surgical/obstetrical fields 12, 13, [15] [16] [17] [18] [47] [48] [49] . We have documented evidence of SARS-CoV-2 RNA in the GI tract, peritoneal cavity, and female genital tract, all of which could potentially be sources of aerosolized virus/viral particles. We did not find evidence of viral RNA in the orthopedic equipment sampled (e.g. saw blade and drill bits), retractors used in cardiac/thoracic surgery and the dermatome used in burn surgery. This may indicate that SARS-CoV-2 does not reside in this type of tissue or at least not present with a viral load high enough for detection.

With our study and others reporting the finding of virus in the peritoneal cavity laparoscopy (and its positive insufflation pressure) theoretically may be considered an aerosol generating procedure justifying the use of appropriate PPE and best practice measures 11, 13, 14, [50] [51] [52] [53] [54] .

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The copyright holder for this preprint this version posted September 7, 2021. ; https://doi.org/10.1101/2021.09.03.21262874 doi: medRxiv preprint

We used standard techniques for air and floor sampling and found evidence of aerosolization of SARS-CoV-2 6, 34, 35, 40, 42 . While the frequency of positive tests was low, this does indicate that aerosolization of the virus does occur in surgery. It is possible that the true positive rates are higher since there are known limitations with the sampling and testing techniques used in this study 6, 34, 35, 40, 42 .

We looked for characteristics of the patients' infections that would increase the risks of detection of viral RNA in the surgical/obstetrical fields or local environment. Higher viral load detected on the initial NP swab (as estimated by the Ct threshold) was associated with a higher risk of detectable virus in our samples, while the subtype of the SARS-CoV-2 virus was not (although the numbers were insufficient for sub-analysis on viral subtyping).

This study was not able to determine if the origin of aerosolized/droplet virus is arising from the surgical fields in the smoke plume. Others did not detect SARS-CoV-2 in electrocautery smoke despite using high viral loads in an in vitro setting 28 . While the lack of any positive viral RNA found on the smoke evacuator filters tested would indicate that the viral contamination from the surgical field is absent or below detection limits, these results cannot be used to definitely conclude that surgical smoke does not harbour SARS-CoV-2.

Since infection with SARS-CoV-2 is primarily via the respiratory tract, we chose to sample the inside of HCWs masks as a means of identifying viral contamination in close proximity to the HCWs respiratory tract. Face mask sampling has previously been shown to be an efficacious way of detecting Mycobacterium tuberculosis contamination 55 and has been used to detect SARS-CoV-2 contamination of masks worn by HCW exposed to COVID-19 infected patients on wards (0/25 positive, inside surface) and directly from patient masks (6/10 positive) 37 . Others have studied SARS-CoV-2 viral contamination on the outer surface of face shields worn by HCWs attending women with COVID-19 in labor (one vaginal delivery with all face shields tested being positive) 35 . We sampled the inside of masks and found 0/143 . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted September 7, 2021. ; https://doi.org/10.1101/2021.09.03.21262874 doi: medRxiv preprint HCWs masks and 0/4 HCWs' face shields to be positive for SARS-CoV-2 RNA. Our study did not detect SARS-CoV-2 RNA on the inner surface of any mask used by HCWs. This is reassuring, since this finding indicates a low risk of HCWs involved with surgery or obstetrical care being exposed to SARS-CoV-2 RNA if using appropriate PPE.

Our study did not include data on the involved HCWs to determine information regarding previous infections or vaccinations, or if they developed subsequent COVID-19 infections.

Detection of SARS-CoV-2 RNA in bioaerosols is recognized to be challenging, being highly dependent upon air flow, exchange rates and source of emissions (reviewed by Borges et al) and it is suggested that parallel sampling with more than one technique may increase sensitivity 56 . Thus, we employed two air sampling techniques, active air sampling used previously by two of our coauthors (finding 3/146 positive air samples taken from patient rooms) 42 and the passive technique similar to what is described by others for SARS-CoV-2 virus 34, 35, 40, 43 .

Despite these efforts, we recognize that it is likely that not all viral contamination was detected with this study. Further, even though viral RNA was detected in some samples, this study did not determine if infectious virus was present.

There is evidence of SARS-CoV-2 RNA in the surgical and obstetrical patient's operative environment (surgical surfaces and aerosolized). However, the finding of no detectable virus on the inner surface of masks worn by the health care teams reassuringly suggests a low risk of infection when wearing appropriate personal protective equipment.

. CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted September 7, 2021. ; https://doi.org/10.1101/2021.09.03.21262874 doi: medRxiv preprint . CC-BY-NC-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted September 7, 2021. ; https://doi.org/10.1101/2021.09.03.21262874 doi: medRxiv preprint 

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on behalf of all members of the NIH/NICHD SARSCoV-2 Placental Infection Workshop. SPECIAL REPORT: A standardized definition of placental infection by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), a consensus statement from the National Institutes of Health/Eunice Kennedy Shriver National Institute of Child Health and Human Development (NIH/NICHD) SARS-CoV-2 placental infection workshop

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