Workplace exposure to carbon dioxide during routine laparoscopy – is it safe ? [ version 2 ; peer review : 1 approved , 1 approved with reservations ]

Background: Minimally invasive surgeries have increased dramatically during the last decades. Carbon dioxide (CO2) is the gas used for insufflation during laparoscopies, creating space and visibility. The CO2 leaks into ambient air through ports where instruments are inserted. If the CO2 reaches a certain concentration it affects personnel health. There are national occupational exposure limits (OEL) for CO2, including a level limit value (LLV) of 5000 ppm. We are not aware of any previous studies addressing occupational exposure to CO2 during laparoscopies. The aim of this study was to assess the compliance to national OELs for CO2 during laparoscopies. Methods: A gas detector was placed in the breathing zone of personnel in the operating theatre. The detector measured CO2 concentrations every tenth minute during laparoscopies in three locations. Results: During 27 laparoscopies, the measured CO2 reached a maximum concentration of 1100 ppm, less than one fourth of the LLV. Median CO2 concentration was 700 ppm. Conclusion: Results show that the occupational exposure to CO2 during laparoscopies is well below set OELs. Our findings support personnel safety associated with routine use of CO2 during laparoscopies.


Introduction
Minimally invasive surgical techniques aim to achieve surgical therapeutic goals with minimal trauma 1 . Minimal invasive surgery (MIS) has increased dramatically and is today well-established for huge numbers of procedures. During all forms of MISs, e.g. classic laparoscopy, gas insufflation is the most commonly used technique to create enough space to allow surgery 2 . The preferred, most commonly used, gas for insufflation is carbon dioxide (CO 2 ) 3 . Characteristics of a perfect gas for insufflation include being colorless, incombustible, easily soluble in blood, non-toxic, inexpensive and easily removed from the body. CO 2 is the gas that best matches these characteristics. To establish a gaseous cushion, an insufflator is used to pump CO 2 into the abdominal cavity or other surgical field. CO 2 will leak into the ambient air from the cavity where the instruments later are inserted, hence the CO 2 concentration in ambient air in the operating theatre may be elevated and thus potentially cause personnel health concern.
Hypercapnia Symptoms of acute hypercapnia include flushed skin, headaches and sweating. Higher CO 2 concentrations in ambient air may also cause anxiety and dizziness. High levels may further cause confusion and shortness of breath and eventually dimmed sight, tremor, unconsciousness or even death 4,5 . The individual response to elevated CO 2 concentrations in ambient air varies depending on the time of exposure and CO 2 concentration 4 .
Recent work suggests that chronic exposure to higher concentration of CO2 may cause negative health effects, potentially having effects on fertility 6,7 .

Occupational exposure limits
To prevent ill health, many countries have provisions regarding the highest acceptable concentrations of air pollutants at workplaces. The highest acceptable average concentration of an air pollutant in workplace air, calculated as time weighted average is known as the occupational exposure limit (OEL). There are two often used OEL values, the level limit value (LLV) and the short-term exposure limit (STEL). LLV is the OEL value for exposure during a working day, normally eight hours. STEL is the OEL value for a reference period of 15 minutes exposure 8 . The Swedish OELs are based on the EU's binding OELs, which includes an LLV of 5000 ppm for CO 2 9 .
The US National Institute for Occupational Safety and Health (NIOSH) has a similar level 10 . The LLV is binding, unlike the STEL for CO 2 at 10000 ppm which is the recommended highest value 8 .
Personnel workplace safety is of huge importance and OELs has been set to secure good working condition, securing personnel health. The workplace CO 2 concentrations may constitute a safety risk. We are not aware of previous studies explicitly addressing the adherence to OELs in operating theatres (OT) during routine use of CO 2 for insufflation during laparoscopies.

Aim
The aim of this study was to assess the occupational exposure to CO 2 in OTs during laparoscopies to verify the compliance to set national (Swedish) OELs.

Study design and context
This was an explorative, non-interventional study of CO 2 concentrations in ambient air during laparoscopies conducted at Danderyd Hospital during October 2019. The CO 2 concentration was measured at three locations: old general surgery ward (OGSW; n=2), new general surgery ward (NGSW; n=1) and day surgery unit (DSU; n=1). The ventilation differed between the locations. In the two older OTs, the air volume flow was 710 L/s (liter/second) and 650 L/s. The air volume flow in the new OT was 2160 L/s during surgeries and 100 L/s during basic ventilation. In the DSU, the air volume flow was between 720 and 2160 L/s.

Surgeries
The laparoscopies included in this study were aggregated into three groups based on the type of surgery: cholecystectomies, hernia repairs and intestinal surgeries. Five groups (A-E) were created depending on the type of surgery and the location: cholecystectomy DSU (A), cholecystectomy NGSW (B), hernia repair NGSW (C), intestinal surgery OGSW (D), intestinal surgery NGSW (E) ( Table 1).

Data collection
A gas detector (TM Dräger X-am 5600, Germany) was used to record point measurements of CO 2 concentrations during the surgeries. This detector has a measurement range of 0-5%, hence the full-scale value is 5% (50000 ppm). The manufacturer of the sensor states an accuracy of ±800 ppm if the CO 2 concentration is 25000 ppm or less. The resolution of the sensor is 100 ppm, thus the scale is divided into 500 equal divisions (400 ppm, 500 ppm, 600 ppm etc.). The exact value displayed depends on the span value set during calibration.
The primary outcome of the study was the concentration of CO 2 in ambient air during MIS. The gas detector was positioned at a height of 153 cm in the OT at the IV pole on the right side of the patient. The CO 2 concentration was noted manually every tenth minute starting on the hour. Observations were collected from the point measurement before the start of

Amendments from Version 1
The manuscript has been revised taking the comments of referee into account.
The average ambient air CO 2 that now exceeds 400 ppm has been added and discussed.
The effective ventilation, air change in operating theatres are further addressed and discussed.
The accuracy of the measuring device is further commented.
Any further responses from the reviewers can be found at the end of the article REVISED surgery until the point measurement after the end of surgery. Start and end of surgery were determined by start-and endpoint as noted by the nurse anesthetist in the medical record.
One of the secondary outcomes was the CO 2 concentration at different heights in the OT. During a laparoscopic hernia repair in the NGSW (group C) the gas detector was placed as previously described. During the first two observations (20 minutes) the detector was placed at a height of 153 cm and was then moved to 105 cm for the next two observations. The following two observations were collected at a height of 15 cm and the detector was then moved back to a height of 153 cm. Observations were collected by changing the height as described every 20 minutes until the end of surgery.
The other secondary outcome of the study was the maximum concentration of CO 2 when gas is allowed to freely enter the OT by disconnecting the insufflation tube from the insufflator. This was conducted in an OT in the NGSW. The gas detector was placed as described previously. The insufflator was set at high flow and the intra-abdominal pressure (IAP) was set to 14 mmHg. The central gas was turned on for five minutes and the highest observed CO 2 concentration, the CO 2 concentrations at the beginning and end of the attempt were noted manually. The attempt was conducted three times, the first time with basic ventilation and the third time with operation ventilation.

Ethical considerations
This was an explorative non-interventional air quality study and the CO 2 concentrations in OTs were monitored only to ensure personnel health. Personnel safety and health is of great importance and this study was significant to assess the personnel safety related to CO 2 in OTs. No patient or personnel data were collected. There was no need for ethical approval. The Head of the Department of Anesthesia and Intensive Care as well as the Head of the Department of Surgery approved the study.

Results
The CO 2 concentration was measured during 20 surgeries where a total of 210 observations were collected with the gas detector. The number of observations in each group ranged from 30 to 57. Possible confounding factors such as the number of people in the OT and IAP showed little variation between groups (Table 1).
During the surgeries, the measured CO 2 concentration showed minor variation. Point measurements from one of the surgeries were selected to show an example of intraoperative variation of CO 2 concentration measured with the gas detector ( Figure 1). During this surgery, 65% of the measured CO 2 concentrations were at 600 ppm and observations ranged from 600 to 1000 ppm. Variation of intraoperative CO 2 concentration was occasionally coherent with emptying and insufflations of gas in the peritoneal cavity. All measured CO 2 concentrations during this surgery were less than or equal to 20% of the LLV (Figure 1).
Out of all observations collected in groups A-E, none exceeded 1100 ppm ( Figure 2). The CO 2 concentration was 600 ppm or 700 ppm in 81% of the observations (Figure 2). Concentration of CO 2 exceeding 700 ppm was seen in 12% of observations.
The CO 2 concentration during the surgeries was measured at 400-1100 ppm and never exceeded 22% of the LLV at 5000 ppm ( Figure 3). Because of the scarce variation in all the groups, sporadic variations are frequently shown as outliers in the box plot.    When the CO 2 concentration was measured at different heights in the OT, results of Kruskal-Wallis test showed no significant difference between heights (χ 2 = 1.371, p = 0.504).
During the three attempts when CO 2 was allowed to freely enter the OT for five minutes, the highest value measured was 2000 ppm. This value is a fifth of the STEL and less than half of the LLV (Figure 4).

Discussion
The primary aim of this study was to measure the concentration of CO 2 in ambient air during laparoscopies to verify compliance to the set national OELs. During 20 laparoscopies in three different locations, the measured CO 2 concentration did not exceed 1100 ppm, which is less than one fourth of the LLV and one ninth of the STEL. Furthermore, when gas was allowed to freely enter the OT for five minutes, mimicking an accidental user error, the measured CO 2 reached a maximum concentration of two fifths of the LLV. Thus, all measured CO 2 concentrations were well below set OELs, hence the findings are reassuring. Our measured vales must be put into perspective. Ambient air CO2 concentration is today higher than ever before, the global average atmospheric carbon dioxide in 2019 was 409.8 parts per million (ppm for short), with a range of uncertainty of plus or minus 0.1 ppm.
Personnel health is of great importance and it is the obligation of all healthcare organizations to secure proper workplace safety including ambient air quality. However, we are not aware of previous studies reporting CO 2 concentrations during laparoscopies. Air quality indices including CO 2 concentrations have nonetheless recently been studied during other types of MIS in a gastrointestinal endoscopy unit 11 . Similar to our findings, the CO 2 concentration in the procedural area was well below set OELs with a median concentration of 593.1 ppm (range 400-1645.9 ppm).
In our study we measured CO 2 as a direct pollutant. Conversely, like the study in the gastrointestinal endoscopy unit, the CO 2 concentration in other hospital environments has previously been studied as an indicator of air quality rather than as a direct pollutant [12][13][14] . The ventilation must thus be taken into account. The ambient air average concentration is today high. Additional CO 2 load, the amount of CO 2 added to the ambient air, CO 2 exhaled by subjects in the room and CO 2 from any additional sources, (e.g. from the insufflation of CO 2 gas) and air change, ventilation, are the main factors for secure ambient air quality. CO 2 as an indicator of air quality has also been studied in other environments such as classrooms 15,16 . Overall, results in these studies of hospital environments and classrooms show concentrations considerably lower than the set OELs. The hospital operating room ventilation is most effective as was shown in our testing extensive leakage, caused by a simulated user error.
The results must be put in perspective of some limitations. The gas detector can only assume certain fixed values, thus small changes in concentration were not detected. Nevertheless, it was important in this study to distinguish between measured CO 2 concentrations and national OELs and detection of smaller changes in CO 2 concentration were not needed for this purpose. The device was calibrated but the accuracy of the instrument must also be acknowledged. Still even in a worst case scenario for accuracy the measured levels are well below OEL. Possible confounding factors include the number of trocars, the ventilation systems, conversion to open surgery, the number of people in the OT and the IAP. Nevertheless, the CO 2 concentration varied little among groups and thus these factors did not seem to have a considerable impact on the concentrations in this study.
Data was handled manually due to the inability to store data and the inability to transfer data to a computer in the gas detector. Concentrations at different heights were only measured during one surgery and differences between heights can therefore not be established. Moreover, concentrations were only measured at one hospital and during rather few surgeries and results may not be generalizable to other hospitals, although all concentrations in the different locations were very low. CO 2 concentrations were only studied at adult surgery departments and because of differences in abdominal cavity volume, amount of CO 2 used and other unrecognized factors, results may be less transferable to children.
In addition, we looked solely at laparoscopies in this study.
Other MIS techniques, such as colonoscopies and robotic surgeries, can be performed in other environments or have a longer duration which might affect CO 2 concentrations.

Conclusion
This study shows that the occupational exposure to CO 2 in OTs during laparoscopies is well below set OELs. Our findings also suggest that CO 2 concentrations are distributed the same way at different heights in the OT. Even when gas is freely entering the OT for five minutes, mimicking an accidental user error, the CO 2 concentrations are well below OELs, hence the results are reassuring. Our findings support personnel safety associated with routine use of CO 2 for insufflation during laparoscopy. The average ambient air CO2 has passed 400 ppm and is today higher than ever before.

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Operating rooms are indeed well ventilated. Merely a rather limited increase was seen in the operating room CO2 concentration when a 5 minute free release of CO2 accident, user error, was mimicked ○ The instrument used was calibrated but the accuracy must of course be acknowledged.

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We have now revised and incorporated these important aspects into the discussion.
Competing Interests: Jan Jakobsson is has a contract with Linde as paid drug safety physician Reviewer Report 13 July 2020 https://doi.org/10.5256/f1000research.26727.r65631 © 2020 Royse C. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Colin F. Royse
Department of Surgery, University of Melbourne, Parkville, Victoria, Australia The authors have conducted a safety study to measure the Carbon Dioxide concentration that could be inhaled by staff in the operating room during laparoscopic surgery.
They chose three different locations, each of which have different ventilation and air volume turnover methodologies. They conducted serial assessments over time for multiple surgeries. They also conducted a brief experiment where they ran CO 2 freely into the operating room.
They found that there is little variance between each of the operating locations or types of surgery. Importantly, all will well below the acceptable limits (level limit value of 5000 PPM). It was interesting, that even the range of CO 2 was relatively small, with the maximum amount being around 1100 PPM. When CO 2 is freely introduced into the air, the values were higherapproximating 2000 PPM, which was still well below the level limit value that is mandated in Europe.
This paper adds to our literature of occupational safety. The use of different theatre locations (old and new) with different air volume turnover rates allows this knowledge to be transferred to other locations and hospitals. It is highly unlikely, even with old theatres, that laparoscopic surgery will produce high levels of carbon dioxide, sufficient to affect health care workers.