Influence of gas type, pressure, and temperature in laparoscopy—a systematic review

Introduction

Laparoscopy is the favoured access to a lot of abdominal operations; for many indications, it is associated with less trauma, faster recovery, reduced costs, similar or better safety, and similar radicality and long-term prognosis in the case of oncologic surgery.

The first step to laparoscopy is to establish a pneumoperitoneum which elevates the abdominal wall and provides for the surgeon’s field of view. This is so natural, that probably most young surgeons do not give a second thought. However, there are reasons for every step of pneumoperitoneum: Why do we use carbon dioxide (CO₂)? Why do not we use simple air or some other gas? Will the patient’s body cool down by the gas? Where does it go? How much pressure do we need? Why do we need pressure? Does it do any damage?

Although laparoscopy was invented more than a hundred years ago and has been, depending on the operation, a routine procedure since the 1980s and 1990s, these questions are not trivial and not completely answered, yet. Following a systematic approach, most questions can be summarised within three categories: gas type, temperature, and pressure. This article aims to explain the rationale behind these topics, summarise the current knowledge, and demonstrate open questions. We present the following article in accordance with the PRISMA reporting checklist (available at https://ales.amegroups.com/article/view/10.21037/ales-21-24/rc).

Methods

For each topic gas type, temperature, and pressure, we give a rationale, why it is important, and which are the theoretical considerations, we declare the specific search string, summarise the results and discuss them.

Separate systematic literature research on MEDLINE for randomized controlled trials (RCT) was performed for each topic as a double-search by both authors. Trials on adults, published between 2011 and March 2021 were considered. The following data were extracted: author, publishing year, trial registry ID, study type, patients, type of surgery, intervention (gas type, temperature, or pressure), comparator, sample size, primary outcomes, secondary outcomes. If the trial did not declare a primary outcome, all outcomes were considered secondary. For each trial we summarise, which comparator was favoured. Current Cochrane reviews with older data were included in the qualitative analysis.

Gas type

Rationale

The ideal gas for a pneumoperitoneum must be cheap, colourless, incombustible, easily removed from the body, non-toxic, and harmless to the patient and the personnel.

Gases that are or have been used, are CO₂, nitrous oxide (N₂O, laughing gas), air, oxygen, nitrogen (N₂), and the inert gases helium (He) and argon (Ar).

CO₂ is the most common and fulfills most of the aforementioned criteria. It is absorbed by the peritoneum, delivered to the lungs via blood, and exhaled. Being a soluble acid, it causes hypercarbia and acidosis, which must be compensated by the anaesthetist by hyperventilation. Hypercarbia can directly decrease cardiac contractility and sensitize the myocardium to arrhythmogenic effects of catecholamines, and indirectly lead to sympathetic stimulation with tachycardia (1). Peritoneal irritation with postoperative pain is reported.

N₂O is rather inert, cheap, and non-flammable, however, it can support combustion (2). In the early days of colonoscopy, there were explosions when electrocautery was used in an unprepared colon. Later, bowel preparation formulas contained mannitol, a substrate for hydrogen-producing bacteria. The fear of flammable colonic gases (methane and hydrogen) mixing up with N₂O during laparoscopy and two case reports of intraoperative explosions from the 1970s lead to the abandonment of N₂O and the recommendation to use CO₂ (3-8). The assumed hemodynamic advantages of N₂O were not evident in the Cochrane reviews. There was low evidence of lower pain scores compared to CO₂, as nitrous oxide is an anaesthetic agent.

CO₂, and—to a lesser extent—nitrous oxide and helium can increase intracranial pressure (9). There is no information on the other gases.

Helium is the least soluble gas for a pneumoperitoneum, potentially increasing the risk of gas embolism. It requires special insufflators.

Ar is another inert gas, more soluble than N₂ and nearly as soluble as air (2).

The generation of trocar metastasis and the influence of the gas are under discussion. Trocar metastases are reported for CO₂ and air pneumoperitoneum, again there is insufficient information for other gases (10). As tumour manipulation by the surgeon, aggressivity of the tumour, and a gas spray effect by the intraabdominal pressure are supposed reasons, port-site metastasis cannot be attributed to the gas type (2).

Gas embolism can occur due to misplacement of a Verres needle into a vein, but also by direct absorption of the gas. Therefore, gases with high solubility are safer. In this respect, CO₂ is superior to N₂O, and both are more soluble than air, oxygen, N₂, and the inert gases He and Ar (1).

All gases can affect the cardiocirculatory, respiratory, and neurohumoral systems by their intraabdominal pressure. These effects are less gas-specific and are discussed in the pressure section.

Methods

MEDLINE was searched through pubmed.gov with the search string: “(((((((((((((((((laparoscop*) OR (video-assisted surgery)) OR (minimally invasive)) OR (coelioscop*)) OR (celioscop*)) OR (peritoneoscop*)) AND (gas type)) OR (carbon dioxide)) OR (CO₂)) OR (nitrous oxide)) OR (laughing gas)) OR (N₂O)) OR (nitrogen)) OR (N₂)) OR (helium)) OR (argon)) AND (pneumoperitoneum)) OR (peritoneum)”. RCTs on adults, published between 2011 and March 2021 were eligible.

Results

We found nine RCTs, of which six had to be excluded because they did not compare CO₂ with another gas, and two because they studied animals or cadavers (Table 1).

The only remaining trial compared CO₂ laparoscopy in general anaesthesia (GC group) with gasless laparoscopy in general anaesthesia (GG group) and gasless laparoscopy in epidural anaesthesia (GE group) (11). The gasless laparoscopy was established with an abdominal lift apparatus. The authors focussed on the stress response, measuring plasma levels of cortisol, TNF‑α, IL-6, IL-10, and Hsp70 before, during, and after the operation. Starting with similar baseline levels in all three groups, the cytokine levels increased most in the GC group, followed by the GG and GE groups. The authors assume that CO₂-laparoscopy induces a larger stress response than gasless techniques, and that general anaesthesia contributes more to stress response than epidural anaesthesia.

The current Cochrane review identified nine RCTs comparing nitrous oxide, helium, and room air to CO₂ with regards to cardiopulmonary complications, surgical morbidity, pneumoperitoneum related serious adverse events (primary endpoints), mortality, quality of life, pain scores, analgesic requirements, costs, and cardiopulmonary changes (secondary outcomes) (12). One trial overlapped with our research. Nitrous oxide was analysed by three trials and exhibited more cardiopulmonary complications (5.7% vs. 2.9%, relative risk ratio 2.0), but the difference was not significant, the trials were heterogeneous and the level of evidence was very low. There were no differences in the other outcomes, either, except for pain levels and analgesia requirements, which were lower with nitrous oxide.

Helium was examined in three trials and exhibited non-significant higher rates of cardiopulmonary complications (4.4% vs. 3.0%) and subcutaneous emphysema (4.9% vs. 0%), and more morphine requirements, but not higher pain scores. The partial blood pressure of CO₂ was lower with helium (−13 mmHg). For room air, only one RCT was found, which did not reveal differences regarding complications and mortality. Costs and pain scores were lower with room air. However, the study quality and consequently the level of evidence were very low.

Discussion

There are many requirements for the ideal gas for a pneumoperitoneum, and none of the gases used are perfect in every aspect. CO₂ has become the standard because it is safe, non-combustible, non-explosive, and cheap. It has some effects on hypercapnia, which is not relevant in cardiopulmonary healthy people, and which the anaesthesiologists have broad experience with and know how to treat.

As the first and only reason to take gas is to improve the surgeon’s field of view, one approach is to completely abandon gas and use mechanical abdominal wall lifting techniques. It is unclear, whether the “no-gas”-study of Han et al. should be attributed to the use of air instead of CO₂ or to the lower intraabdominal pressure by an abdominal wall lifting technique. The influence of pressure is discussed in the next section. Furthermore, abdominal wall lifting is a quite invasive tool to be combined with minimally invasive surgery.

No recent data is expanding the results of the Cochrane reviews of 2013 and 2017 (12,13). There is a lack of effort in testing inert gases like He or Ar against the standard, especially with regards to safety. One risk is gas embolism. CO₂ is safer than oxygen, nitrous oxide, and room air in animal studies, because of its solubility. However, as venous gas embolism is rare, larger scaled meta-analyses will be necessary to provide better safety evidence. Cardiopulmonary changes due to CO₂ that we discussed in the rationale are only relevant in patients with pre-existing diseases. As there is broad experience with the properties of CO₂ and the handling of its disadvantages, it seems, at first sight, that there is no need for alternatives to CO₂. To establish another gas, more high-quality RCTs and meta-analyses are necessary. For which gas should we take these efforts?

For low-income countries, the use of filtered room air promises lower costs. The higher cost-effectiveness of air has been shown (14). However, room air has the narrowest data basis of all gases. From the author’s point of view, perhaps more academic efforts should be directed towards room air.

Temperature

Rationale

CO₂ is stored in a compressed and liquid state at about −90 °C. When released, it expands rapidly and enters the patient’s body at room temperature with no humidity. Cold CO₂ is therefore supposed to cool the body and expose the patient to hypothermia which can cause coagulopathies and alter drug metabolism. However, calorimetric calculations have demonstrated that hundreds of litres of cold dry CO₂ will have hardly any impact on the patient’s core temperature (far below 0.5 °C) (15).

Dry CO₂ is discussed to damage mesothelial cells (16), leading to peritoneal inflammation, which is assumed to contribute to postoperative pain and the long-time forming of peritoneal adhesions. More adhesions were found in animal models (17).

Methods

MEDLINE was searched via pubmed.gov with the search string: “(((((((laparoscop*) OR (coelioscop*)) OR (celioscop*)) OR (peritoneoscop*)) OR (minimally invasive)) OR (video assisted surgery)) AND (temperature OR therm*)) AND (pneumoperitoneum)”. RCTs on adults, published from 2011 to March 2021 were eligible.

Results

We identified only four RCTs, one of which with only the abstract, as the full text was in the Russian language (Table 2). We, therefore, decided to include one RCT on children (age 8–14 years) with appendectomies. All studies compared warm humidified (WH; 37 °C and 95–98% humidity) with cool dry (CD; 20 °C, 0%) CO₂.

Agaev et al. found fewer pain scores and the need for analgesics in the WH in 150 laparoscopic operations (cholecystectomies and fundoplications); however, we could not access the full text since it was published in the Russian language (18).

Jiang et al. compared WH with two CD-groups; one had external warming with electric (CE) and one with forced heated air blankets (CF). They included only elderly patients with colorectal surgery. Pain scores were similar in WH and CE, but higher in CF. The same constellation was found for intraoperative hypothermia, coagulation dysfunction, early postoperative cough pain, sufentanil consumption, days to first flatus and solid food intake, and length of hospital stay. The authors attribute the differences to insufficient maintenance of normothermia in the group with electric blankets and emphasize the necessity of normothermia. WH and CD with forced heated air blankets were equivalent in this trial (19).

Sammour et al. published a five-year follow-up of a randomized trial of 2010 (23), focussing on the long-term effects of small bowel obstruction as representative of adhesions, local tumour recurrence, overall and cancer-specific survival (20). There were no differences between WH and CD. Small bowel obstruction occurred in 5.6% of WH and 0% of CD patients (P=0.2). One should consider that on one hand, small bowel obstruction is not the only surrogate of adhesions, on the other hand, it can have other reasons than adhesions, for example, anastomotic stenosis.

Sutton et al. combined clinical and experimental outcomes (21). In a subgroup of 42 of 101 patients, they took peritoneal samples at the start and at the end of the operation, which were compared histologically. They found fewer histologic alterations in the end-of-operation specimens in the WH group compared to the CD group, but the difference was not statistically significant. Postoperative plasma levels of cytokines did not differ between WH and CD, either. The WH group needed fewer narcotics and early postoperative analgetic medication, although the pain scores were similar. The authors state not to draw “firm conclusions … regarding the use of pain medications”. There were no differences in clinical outcome parameters length of stay, complication rates, time of flatus, and time of diet.

Yu et al. performed a large-scaled RCT on appendectomies in children, revealing no differences in postoperative opioid consumption, pain scores, intraoperative core body temperature, postoperative recovery, and return to normal activities (22).

A current Cochrane analysis summarises the current knowledge up to 2016 (24): the authors found 22 randomized trials, four of which overlapped with our search. The intraoperative body core temperature was 0.31 °C higher in the warm, humidified CO₂ group; however, when studies with a moderate or high risk of bias were excluded, this difference was not statistically significant. Postoperative pain scores did not differ between the warm and cold groups. Morphine use at the first and second postoperative days was similar in the cold and warm, humidified groups, but higher in the warm, not humidified CO₂ group. The postoperative recovery time did not differ when the only high risk of bias study was excluded from the analysis. Length of hospital stay and recovery time were similar in all groups.

Discussion

Since up to several hundred litres of gas flow through the abdomen during the operation, it is reasonable to assume that the gas should have a relevant influence on core body temperature and the body’s moisture homeostasis. However, the clinical studies demonstrate that the body temperature is not impaired by CD in a clinically relevant manner. The clinical trials recording the core temperature found only minimal changes which fit very well to the theoretical calorimetric calculations of Roth et al. (15). The Cochrane analysis did not find significant differences in postoperative pain scores and the need for analgesic medication, and the few recent trials published after the Cochrane review are heterogeneous, not favouring WH gas. Short-time clinical outcomes are not influenced by WH or CD, either.

There is hardly any evidence of the formation of adhesions due to the use of WH or CD gas. It is always difficult to measure the effectiveness of an intervention on the forming of adhesions within a human clinical trial, as the generation of adhesions is multifactorial and difficult to quantify. Even animal autopsy trials do not allow to conclude from the morphologic evidence of adhesions on their clinical relevance. Thus, although there is a clinical long-term follow-up RCT, the data are insufficient to judge the impact of WH and CD on adhesions.

In conclusion, there is no evidence for the use of WH gas. The decision to use WH should be drawn based on the local availability, since warming and humidifying CO₂ is related to additional costs.

Pressure

Rationale

A pneumoperitoneum, and therefore pressure, is necessary to elevate the abdominal wall from the organs to provide for the surgeon’s field of view. Even abdominal wall lifting techniques which avoid a classic pneumoperitoneum, aim to establish the field of view.

The pressure on the peritoneum, however, reduces the blood flow in the low-pressure vessels, capillaries, and veins, which could contribute to inflammatory or stress response. It also affects the vasopressin and renin-angiotensin-aldosterone-system (25). The pressure on the liver (veins), diaphragm, and lung can reduce the cardiac preload, the lung volume by about one-third, provoke atelectasis, shunt, and ventilation-perfusion-mismatch.

Thus, it seems desirable to reduce the pressure to minimize cardiopulmonary complications, and simultaneously find the balance to still provide a good field of view.

Methods

MEDLINE was searched through pubmed.gov with the string: “(((((((laparoscop*) OR (coelioscop*)) OR (celioscop*)) OR (peritoneoscop*)) OR (minimally invasive)) OR (video assisted surgery)) AND (pressure)) AND (pneumoperitoneum)”. The search was limited to randomised clinical trials from 2010 to March 2021. Trials on children, animals, or cadavers were excluded. In contrast to the Cochrane review, all kinds of laparoscopic operations were considered.

Results

Thirty-eight RCTs were identified (Table 3). Nine trials were excluded: three were study protocols, three were not randomised trials, three were trials on children. Most RCTs compared low pressure (LP, about 8 mmHg) with standard (SP, about 12 mmHg) or high pressure (HP, >15 mmHg); these categories were quite homogenous.

Six trials focussed on the effect of deep compared to standard neuromuscular blockade (NMB) to facilitate a lower intraabdominal pressure (37,38,41,47,53,54). The outcomes of these NMB-studies focussed on the surgeon’s conditions (space, field of view, surgeon’s satisfaction) in four trials, all favouring deep NMB (41,47,53,54), intraocular pressure, and intraabdominal contractions (38,53), both favouring deep NMB. General and patient-related outcomes (pain, emesis, opioid consumption, length of stay, etc.) did not differ between deep and normal NMB combined with low-pressure peritoneum.

All eight trials focussing on postoperative pain or analgesic consumption favoured LP (28,34,37,46,49-52). Experimental or biochemical studies revealed an improved peritoneal perfusion in the LP group (27,32), less histological damage in renal tubules (26), partially less elevation of liver enzymes (30,33,40), less inflammatory blood markers (26,31,39). The impact on coagulation was heterogeneous in two studies [(44), no difference; (48), impaired thrombelastography in HP; (49), more haemorrhage in HP]. The femoral vein diameter and blood flow were better in LP group (44).

Only two trials measured respiratory parameters: maximal values of peak airway pressure, end-tidal CO_2, and systolic blood pressure were lower in the LP group at Sroussi et al. (46), base excess and bicarbonate were higher with HP, but within normal limits at Hypolito et al. (35). The LP group had higher urine output, but no difference in creatinine serum levels (52).

Quality of recovery as a patient-related outcome was assessed by two RCTs with no landmark results (XX).

The Cochrane review of 2014 identified 21 RCTs comparing low with standard pressure in patients with laparoscopic cholecystectomy. Nineteen of these trials were older than 2011 and did not overlap with our search. Primary outcomes were mortality, serious adverse events, and quality of life, secondary outcomes were conversion to open cholecystectomy, hospital stay, return to normal activity, return to work, operating time. There was no mortality, no differences in serious adverse events. Quality of life and return to work or normal activities were not reported in any of the trials. Length of stay was not significantly different, operating time was 2 minutes longer in the LP group.

Discussion

The reason to use gas is to form a space between abdominal wall and organs to provide for the surgeon’s field of view and action. This space enables the operation and also ensures the safety of the patient. However, pressure on the organs is inevitable. The potential effects of pressure are numerous: Capillary and venous blood flow, gut motility, autonomous nerve system, etc.

While the Cochrane review focussed on clinical outcomes of one specific, ubiquitous surgical procedure, i.e., cholecystectomy, our search involved all laparoscopic operations and non-clinical outcomes, too. These trials confirmed differences, which have been deducted from the theoretical considerations: peritoneal perfusion and inflammatory responses are better in the LP group because the low pressure impairs the capillary and venous blood flow less. Following the same logic, urine output and liver enzymes are impaired by higher intraabdominal pressure. Unfortunately, the impact on the organs “beyond the diaphragm”, circulation and respiration, is hardly reflected by most of the trials.

However, these statistically significant differences do not translate into clinical relevance, as shown by the Cochrane review. The only clinical difference which has been confirmed is reduced shoulder pain after cholecystectomy. In contrast to this advantage for the patient, there is the surgeon’s discomfort with LP. Although this discomfort did not translate into an increased rate of morbidity for the patient, the surgical field of view should not only be considered as the surgeon’s comfort but also as a relevant factor for the patient’s safety. Furthermore, the low morbidity reported by the Cochrane review corresponds with a rather healthy patient population. Consequently, the authors state that the data do not allow inferences on the impact of LP on a patient with cardiopulmonary comorbidities and that information on the safety of LP is lacking. Recent trials demonstrated that a deeper neuromuscular blockade can facilitate laparoscopy with low pressure. Future trials should focus on patients with comorbidities and high anaesthetical risk and specifically analyse the clinical impact on circulation and respiration.

Summary

CO₂ is the preferred gas to establish a pneumoperitoneum. Although it has some drawbacks like hypercapnia and acidosis especially in cardiorespiratory diseased patients, there is a broad experience in anaesthesiologic techniques which compensate for its disadvantages. Nitrous oxide has a desirable anaesthetic effect, is also cheap and available, but it does not suffocate combustion. The necessity of this suffocating effect is under discussion. Other gases like He, Ar, N₂, and room air are not sufficiently tested for their safety. Room air could be desirable for low-income countries as it is the most cost-effective gas, so more efforts to investigate air for pneumoperitoneum are needed.

The use of warm humidified instead of cold dry CO₂ has no benefit but is associated with higher costs.

The potential benefit of low-pressure peritoneum on possible cardiovascular and respiratory complications could not be demonstrated as most trials focus on low-risk patients. It decreases shoulder pain after cholecystectomy. However, low-pressure peritoneum impairs the surgical field of view. At the moment, there is no benefit from using low instead of standard pressure.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editors (Philipp Lingohr and Jonas Dohmen) for the series “Immunologic Implications of Minimal Invasive Surgery” published in Annals of Laparoscopic and Endoscopic Surgery. The article has undergone external peer review.

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://ales.amegroups.com/article/view/10.21037/ales-21-24/rc

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://ales.amegroups.com/article/view/10.21037/ales-21-24/coif). The series “Immunologic Implications of Minimal Invasive Surgery” was commissioned by the editorial office without any funding or sponsorship. The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Gutt CN, Oniu T, Mehrabi A, et al. Circulatory and respiratory complications of carbon dioxide insufflation. Dig Surg 2004;21:95-105. [Crossref] [PubMed]
2. Menes T, Spivak H. Laparoscopy: searching for the proper insufflation gas. Surg Endosc 2000;14:1050-6. [Crossref] [PubMed]
3. Hunter JG, Staheli J, Oddsdottir M, et al. Nitrous oxide pneumoperitoneum re-visited. Is there a risk of combustion? Surg Endosc 1995;9:501-4. [Crossref] [PubMed]
4. Gallagher EA, Clarke E, Connor M, et al. A study of intracolonic hydrogen and methane levels during colonoscopy. Ir J Med Sci 1992;161:582-5. [Crossref] [PubMed]
5. Ladas SD, Karamanolis G, Ben-Soussan E. Colonic gas explosion during thera-peutic colonoscopy with electrocautery. World J Gastroenterol 2007;13:5295-8. [Crossref] [PubMed]
6. La Brooy SJ, Avgerinos A, Fendick CL, et al. Potentially explosive colonic concentrations of hydrogen after bowel preparation with mannitol. Lancet 1981;1:634-6. [Crossref] [PubMed]
7. Gunatilake DE. Case report: fatal intraperitoneal explosion during electrocoag-ulation via laparoscopy. Int J Gynaecol Obstet 1978;15:353-7. [Crossref] [PubMed]
8. El-Kady AA, Abd-El-Razek M. Intraperitoneal explosion during female sterili-zation by laparoscopic electrocoagulation. A case report. Int J Gynaecol Obstet 1976;14:487-8. [Crossref] [PubMed]
9. Schöb OM, Allen DC, Benzel E, et al. A comparison of the pathophysiologic effects of carbon dioxide, nitrous oxide, and helium pneumoperitoneum on intra-cranial pressure. Am J Surg 1996;172:248-53. [Crossref] [PubMed]
10. Safran DB, Orlando R 3rd. Physiologic effects of pneumoperitoneum. Am J Surg 1994;167:281-6. [Crossref] [PubMed]
11. Han C, Ding Z, Fan J, et al. Comparison of the stress response in patients un-dergoing gynecological laparoscopic surgery using carbon dioxide pneumoperito-neum or abdominal wall-lifting methods. J Laparoendosc Adv Surg Tech A 2012;22:330-5. [Crossref] [PubMed]
12. Yu T, Cheng Y, Wang X, et al. Gases for establishing pneumoperitoneum during laparoscopic abdominal surgery. Cochrane Database Syst Rev 2017;6:CD009569. [Crossref] [PubMed]
13. Cheng Y, Lu J, Xiong X, et al. Gases for establishing pneumoperitoneum during laparoscopic abdominal surgery. Cochrane Database Syst Rev 2013;CD009569. [PubMed]
14. O’Connor Z, Faniriko M, Thelander K, et al. Laparoscopy Using Room Air In-sufflation in a Rural African Jungle Hospital: The Bongolo Hospital Experience, January 2006 to December 2013. Surg Innov 2017;24:264-7. [Crossref] [PubMed]
15. Roth JV, Sea S. An assessment by calorimetric calculations of the potential thermal benefit of warming and humidification of insufflated carbon dioxide. Surg Laparosc Endosc Percutan Tech 2014;24:e106-9. [Crossref] [PubMed]
16. Liu Y, Hou QX. Effect of carbon dioxide pneumoperitoneum during laparo-scopic surgery on morphology of peritoneum. Zhonghua Yi Xue Za Zhi 2006;86:164-6. [PubMed]
17. Peng Y, Zheng M, Ye Q, et al. Heated and humidified CO2 prevents hypother-mia, peritoneal injury, and intra-abdominal adhesions during prolonged laparoscopic insufflations. J Surg Res 2009;151:40-7. [Crossref] [PubMed]
18. Agaev BA, Muslimov GF, Ibragimov TR, et al. The efficacy of the moisture and warmed CO(2) for laparoscopic surgery. Khirurgiia (Mosk) 2013;35-9. [PubMed]
19. Jiang R, Sun Y, Wang H, et al. Effect of different carbon dioxide (CO2) insuf-flation for laparoscopic colorectal surgery in elderly patients: A randomized con-trolled trial. Medicine (Baltimore) 2019;98:e17520. [Crossref] [PubMed]
20. Sammour T, Hill AG. Five year follow-up of a randomized controlled trial on warming and humidification of insufflation gas in laparoscopic colonic sur-gery--impact on small bowel obstruction and oncologic outcomes. Int Surg 2015;100:608-16. [Crossref] [PubMed]
21. Sutton E, Bellini G, Grieco MJ, et al. Warm and Humidified Versus Cold and Dry CO2 Pneumoperitoneum in Minimally Invasive Colon Resection: A Random-ized Controlled Trial. Surg Innov 2017;24:471-82. [Crossref] [PubMed]
22. Yu TC, Hamill JK, Liley A, et al. Warm, humidified carbon dioxide gas insuf-flation for laparoscopic appendicectomy in children: a double-blinded randomized controlled trial. Ann Surg 2013;257:44-53. [Crossref] [PubMed]
23. Sammour T, Kahokehr A, Hayes J, et al. Warming and humidification of in-sufflation carbon dioxide in laparoscopic colonic surgery: a double-blinded ran-domized controlled trial. Ann Surg 2010;251:1024-33. [Crossref] [PubMed]
24. Birch DW, Dang JT, Switzer NJ, et al. Heated insufflation with or without hu-midification for laparoscopic abdominal surgery. Cochrane Database Syst Rev 2016;10:CD007821. [PubMed]
25. Ott DE. Subcutaneous emphysema--beyond the pneumoperitoneum. JSLS 2014;18:1-7. [Crossref] [PubMed]
26. Aditianingsih D, Mochtar CA, Lydia A, et al. Effects of low versus standard pressure pneumoperitoneum on renal syndecan-1 shedding and VEGF receptor-2 expression in living-donor nephrectomy: a randomized controlled study. BMC Anesthesiol 2020;20:37. [Crossref] [PubMed]
27. Albers KI, Polat F, Loonen T, et al. Visualising improved peritoneal perfusion at lower intra-abdominal pressure by fluorescent imaging during laparoscopic surgery: A randomised controlled study. Int J Surg 2020;77:8-13. [Crossref] [PubMed]
28. Ali IS, Shah MF, Faraz A, Khan M. Effect of intra-abdominal pressure on post-laparoscopic cholecystectomy shoulder tip pain: A randomized control trial. J Pak Med Assoc 2016;66:S45-9. [PubMed]
29. Barrio J, Errando CL, García-Ramón J, et al. Influence of depth of neuromus-cular blockade on surgical conditions during low-pressure pneumoperitoneum lap-aroscopic cholecystectomy: A randomized blinded study. J Clin Anesth 2017;42:26-30. [Crossref] [PubMed]
30. Chang-Sheng H, Chong-Yao B, Hong-Yi Y, et al. Effects of varied pneu-moperitoneal pressure on liver biochemistries following laparoscopic cholecystec-tomy. Clin Res Hepatol Gastroenterol 2012;36:e38-9. [Crossref] [PubMed]
31. Díaz-Cambronero O, Mazzinari G, Flor Lorente B, et al. Effect of an individu-alized versus standard pneumoperitoneum pressure strategy on postoperative re-covery: a randomized clinical trial in laparoscopic colorectal surgery. Br J Surg 2020;107:1605-14. [Crossref] [PubMed]
32. Eryılmaz HB, Memiş D, Sezer A, et al. The effects of different insufflation pressures on liver functions assessed with LiMON on patients undergoing laparo-scopic cholecystectomy. ScientificWorldJournal 2012;2012:172575. [Crossref] [PubMed]
33. Gupta R, Kaman L, Dahiya D, et al. Effects of varying intraperitoneal pressure on liver function tests during laparoscopic cholecystectomy. J Laparoendosc Adv Surg Tech A 2013;23:339-42. [Crossref] [PubMed]
34. Hsu KF, Chen CJ, Yu JC, et al. A Novel Strategy of Laparoscopic Insufflation Rate Improving Shoulder Pain: Prospective Randomized Study. J Gastrointest Surg 2019;23:2049-53. [Crossref] [PubMed]
35. Hypolito O, Azevedo JL, Gama F, et al. Effects of elevated artificial pneu-moperitoneum pressure on invasive blood pressure and levels of blood gases. Braz J Anesthesiol 2014;64:98-104. [Crossref] [PubMed]
36. Ko-Iam W, Paiboonworachat S, Pongchairerks P, et al. Combination of etoricoxib and low-pressure pneumoperitoneum versus standard treatment for the management of pain after laparoscopic cholecystectomy: a randomized controlled trial. Surg Endosc 2016;30:4800-8. [Crossref] [PubMed]
37. Madsen MV, Istre O, Staehr-Rye AK, et al. Postoperative shoulder pain after laparoscopic hysterectomy with deep neuromuscular blockade and low-pressure pneumoperitoneum: A randomised controlled trial. Eur J Anaesthesiol 2016;33:341-7. [Crossref] [PubMed]
38. Madsen MV, Istre O, Springborg HH, et al. Deep neuromuscular blockade and low insufflation pressure during laparoscopic hysterectomy. Dan Med J 2017;64:A5364. [PubMed]
39. Matsuzaki S, Vernis L, Bonnin M, et al. Effects of low intraperitoneal pressure and a warmed, humidified carbon dioxide gas in laparoscopic surgery: a randomized clinical trial. Sci Rep 2017;7:11287. [Crossref] [PubMed]
40. Neogi P, Kumar P, Kumar S. Low-pressure Pneumoperitoneum in Laparoscopic Cholecystectomy: A Randomized Controlled Trial. Surg Laparosc Endosc Percutan Tech 2020;30:30-4. [Crossref] [PubMed]
41. Özdemir-van Brunschot DMD, Braat AE, van der Jagt MFP, et al. Deep neu-romuscular blockade improves surgical conditions during low-pressure pneu-moperitoneum laparoscopic donor nephrectomy. Surg Endosc 2018;32:245-51. [Crossref] [PubMed]
42. Özdemir-van Brunschot DMD, Scheffer GJ, van der Jagt M, et al. Quality of Recovery After Low-Pressure Laparoscopic Donor Nephrectomy Facilitated by Deep Neuromuscular Blockade: A Randomized Controlled Study. World J Surg 2017;41:2950-8. Erratum in: World J Surg 2017 Aug 18. [Crossref] [PubMed]
43. Schietroma M, Carlei F, Cecilia EM, et al. A prospective randomized study of systemic inflammation and immune response after laparoscopic nissen fundoplica-tion performed with standard and low-pressure pneumoperitoneum. Surg Laparosc Endosc Percutan Tech 2013;23:189-96. [Crossref] [PubMed]
44. Sharma A, Dahiya D, Kaman L, et al. Effect of various pneumoperitoneum pressures on femoral vein hemodynamics during laparoscopic cholecystectomy. Updates Surg 2016;68:163-9. [Crossref] [PubMed]
45. Shoar S, Naderan M, Ebrahimpour H, et al. A prospective double-blinded ran-domized controlled trial comparing systemic stress response in Laparoascopic cholecystectomy between low-pressure and standard-pressure pneumoperitoneum. Int J Surg 2016;28:28-33. [Crossref] [PubMed]
46. Sroussi J, Elies A, Rigouzzo A, et al. Low pressure gynecological laparoscopy (7 mmHg) with AirSeal® System versus a standard insufflation (15 mmHg): A pilot study in 60 patients. J Gynecol Obstet Hum Reprod 2017;46:155-8. [Crossref] [PubMed]
47. Staehr-Rye AK, Rasmussen LS, Rosenberg J, et al. Surgical space conditions during low-pressure laparoscopic cholecystectomy with deep versus moderate neu-romuscular blockade: a randomized clinical study. Anesth Analg 2014;119:1084-92. [Crossref] [PubMed]
48. Topal A, Celik JB, Tekin A, et al. The effects of 3 different intra-abdominal pressures on the thromboelastographic profile during laparoscopic cholecystectomy. Surg Laparosc Endosc Percutan Tech 2011;21:434-8. [Crossref] [PubMed]
49. Topçu HO, Cavkaytar S, Kokanalı K, et al. A prospective randomized trial of postoperative pain following different insufflation pressures during gynecologic laparoscopy. Eur J Obstet Gynecol Reprod Biol 2014;182:81-5. [Crossref] [PubMed]
50. Vijayaraghavan N, Sistla SC, Kundra P, et al. Comparison of standard-pressure and low-pressure pneumoperitoneum in laparoscopic cholecystectomy: a double blinded randomized controlled study. Surg Laparosc Endosc Percutan Tech 2014;24:127-33. [Crossref] [PubMed]
51. Warlé MC, Berkers AW, Langenhuijsen JF, et al. Low-pressure pneumoperi-toneum during laparoscopic donor nephrectomy to optimize live donors’ comfort. Clin Transplant 2013;27:E478-83. [Crossref] [PubMed]
52. Yasir M, Mehta KS, Banday VH, et al. Evaluation of post operative shoulder tip pain in low pressure versus standard pressure pneumoperitoneum during laparo-scopic cholecystectomy. Surgeon 2012;10:71-4. [Crossref] [PubMed]
53. Yoo YC, Kim NY, Shin S, et al. The Intraocular Pressure under Deep versus Moderate Neuromuscular Blockade during Low-Pressure Robot Assisted Laparo-scopic Radical Prostatectomy in a Randomized Trial. PLoS One 2015;10:e0135412. [Crossref] [PubMed]
54. Koo BW, Oh AY, Seo KS, et al. Randomized Clinical Trial of Moderate Versus Deep Neuromuscular Block for Low-Pressure Pneumoperitoneum During Laparo-scopic Cholecystectomy. World J Surg 2016;40:2898-903. [Crossref] [PubMed]