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. 2022 Apr;63(4):416–421.

The effect of laparoscopy on intracranial pressure as measured by optic nerve sheath diameter: A review

Kevin G Mitchell 1, Ryan B Appleby 1,✉, Melissa D Sinclair 1, Ameet Singh 1
PMCID: PMC8922386  PMID: 35368391

Abstract

Laparoscopic surgery has many benefits over open surgery including lower complication rates, and shorter duration and lower cost of hospitalization. However, recent human literature suggests laparoscopy and carbon dioxide insufflation can result in intracranial hypertension. Invasive monitoring of intracranial pressure is not routinely performed in veterinary medicine, and ultrasonographic evaluation of the optic nerve sheath has been employed as an indirect measure of intracranial pressure in many species. The optic nerve sheath is continuous with the meninges of the brain and becomes distended with intracranial hypertension. Optic nerve sheath diameter is a reliable and consistent measure of intracranial pressure and has been utilized in humans to evaluate patients for intracranial hypertension secondary to laparoscopy and capnoperitoneum. No thorough evaluation of the effects of laparoscopy on intracranial pressure has been performed in dogs. Ultrasonographic evaluation of the optic nerve sheath is a safe, non-invasive, and inexpensive procedure that may allow for the evaluation of intracranial pressure without the need for invasive monitoring systems. As laparoscopic procedures are performed increasingly often, this review aims to inform the reader on the effects of capnoperitoneum and to facilitate appropriate patient selection, anesthetic considerations, and surgical planning.

Introduction

Laparoscopy was invented during the turn of the 20th century by the German surgeon Georg Kelling, who developed trocharization and oxygen insufflation techniques in the canine model (1). By 1910, the Swedish internist Hans Christian Jacobaeus was performing these procedures in humans (1). Dr. Jacobaeus is an important figure in pioneering the advancement of laparoscopic techniques, and is also credited with stressing the importance of understanding their inherent limitations (1). As laparoscopic procedures continued to be developed and refined over the past century, carbon dioxide (CO2) insufflation became standard practice in most instances (2). Carbon dioxide is inexpensive, odorless, colorless, noninflammable, and can be easily removed from the bloodstream over time, making it an ideal choice over alternatives such as helium, oxygen (O2), or nitrous oxide (N2O) (2).

Laparoscopic procedures in humans are associated with decreased pain and a quicker recovery time, and although appropriate patient selection is paramount for success, laparoscopic procedures have been associated with decreased estimated blood loss and decreased complication rates (3–5). A retrospective analysis in humans comparing laparoscopic and open approaches to 6 common surgical procedures revealed laparoscopy to be superior in almost all facets, including reduced mortality and reduced hospital readmissions (5). Due to their minimally invasive nature, these procedures are commonly associated with reduced hospitalization time and a reduction in overall cost of hospitalization (5,6).

Despite the proposed benefits of laparoscopy, these procedures are not without drawbacks and associated complications. The increased intracranial pressure associated with this procedure has been assessed over the past several decades in humans but has not been thoroughly evaluated in dogs (7). Invasive monitoring devices for intracranial pressure are not routinely used in veterinary medicine, and the effects of laparoscopic insufflation on intracranial pressure remains uncharacterized in dogs. Increased intracranial pressure can lead to ischemic injury of neurons and a cascade of cellular edema and free radical production (8). The ultrasonographic assessment of the optic nerve sheath diameter (ONSD) appears to offer a reliable indirect measurement of intracranial pressure in many different species, including dogs (8). This literature review aims to highlight some of the known effects of laparoscopic insufflation with a primary focus on increased intracranial pressure. The measurement of the optic nerve sheath diameter will be discussed in both animals and humans as a surrogate measure of intracranial pressure to help guide future research and more definitively determine whether invasive monitoring is necessary in veterinary medicine.

Materials and methods

A literature search was performed using the PubMed database and employing the search terms laparoscopy, intracranial pressure, and optic nerve sheath diameter, which generated articles from years 2014 to 2020. No veterinary specific literature was generated in this search. Additional literature was included based upon topic relevance. All articles were assessed for their content and applicability to the proposed research opportunity, specifically with regard to ultrasonographic measurement of ONSD to indirectly measure intracranial pressure changes throughout laparoscopic capnoperitoneum.

Results

The initial literature search revealed 22 articles from the human literature, which matched the proposed criteria consisting of clinical trials, randomized controlled trials, and a systematic review and meta-analysis. A single editorial comment was also generated and excluded from the review. The scope of the literature search was expanded to include additional articles, such as studies using animal models to discuss the effects of laparoscopic insufflation and veterinary-specific articles discussing the measurement of the optic nerve sheath. These articles were retrieved and reviewed based on relevance and level of contribution to the field. Species-specific veterinary articles using canine, feline, and equine models as well as several animal research articles in pigs were recruited.

Laparoscopic insufflation and capnoperitoneum

The cardiovascular effects of capnoperitoneum have been assessed in dogs. Williams and Murr (9) investigated the effects of laparoscopic insufflation on cardiopulmonary function. In that study, cardiac output and stroke volume were decreased to < 80% of baseline values with peritoneal insufflation. The Trendelenburg position during surgery (patient supine, feet 15° above head) was used to protect against the depression of cardiac function to a substantial degree at lower intraabdominal pressures. The depression of cardiac function was hypothesized to be secondary to increased venous pressure and venous return (9). However, Duke et al (10) further investigated the cardiopulmonary effects of capnoperitoneum in dogs and saw no significant changes in cardiac output at lower intraabdominal pressures. In 5 dogs undergoing general anesthesia with controlled ventilation and the maintenance of end-tidal CO2, cardiac output was suspected to be maintained through compensatory increases in heart rate despite any mild alterations in stroke volume and systemic vascular resistance (10).

The effects of hypercapnia secondary to capnoperitoneum and the mechanical pressure associated with gas insufflation have been explored in multiple studies using pigs throughout the 1990’s. In a comparison between helium and CO2 insufflation in swine, Leighton et al (11) showed that capnoperitoneum promoted respiratory acidosis and an increased arterial partial pressure of carbon dioxide (PCO2) despite mechanical ventilation. These effects were not noted with helium insufflation, as helium appears to be minimally absorbed within the peritoneal space (11). Leighton et al (11) hypothesized that this was only partially related to perfusion, as hypercapnia persisted throughout iatrogenically induced hemorrhagic shock and marked hypotension. Each of these 8 patients were assessed under 3 sequential conditions (helium insufflation, CO2 insufflation, and CO2 insufflation with hemorrhagic shock) throughout the same anesthetic period and no strict control group was present.

A series of experimental animal studies were performed over the following few years, which attempted to characterize the hemodynamic changes associated with laparoscopy including systemic and pulmonary arterial hypertension and a reduction in stroke volume (12,13). In 1993, the effect of capnoperitoneum on hemodynamically compromised animals was expanded upon by Ho et al (12) in a randomized clinical trial. Hypercapnia and acidemia secondary to capnoperitoneum were repeatable findings regardless of the degree of hemorrhage and fluid resuscitation in this population of pigs (12). A marked reduction in stroke volume was seen with capnoperitoneum alone, and patients receiving fluid resuscitation after hemorrhage appeared less responsive to fluid therapy with capnoperitoneum (12). Another study by the same authors published in 1995 demonstrated that some of these hemodynamic changes and acid-base disturbances were not present in a control group that used nitrogen gas insufflation (13). Expired airflow analysis with a metabolic measurement cart was performed in 8 adult pigs undergoing laparoscopy, and Ho et al (13) showed a 75% increase in the pulmonary excretion of CO2 when this gas was used for insufflation. This indicates that the metabolic changes and hemodynamic compromise are related to systemic CO2 absorption rather than the mechanical pressure of insufflation, as these changes were not noted with pneumoperitoneum established with nitrogen gas (13).

Subsequent studies in porcine models revealed that, regardless of the gas used for insufflation, the acid-base compensatory mechanisms are likely at least partly dependent upon the intraabdominal insufflation pressure and that excessive intraabdominal pressure can lead to catecholamine surges and further compromise in hemodynamics (14,15). Mikami et al (15) replicated the arterial PCO2 increase with capnoperitoneum that was not noted with air or nitrous oxide and demonstrated that an increased intraabdominal pressure alone can increase the plasma concentration of catecholamines regardless of the type of gas used. Although epinephrine and norepinephrine were expected to be increased in the CO2 insufflation group due to hypercapnia, these changes were also seen throughout all other groups when the intraabdominal pressure was increased to 20 mmHg (15). Mikami et al (15) hypothesized these changes to be secondary to vessel collapse from the intraabdominal pressure, leading to decreased venous return, decreased cardiac output and stimulation of the sympathetic nervous system. The tracheotomy, cystostomy, and peritoneal trocarization performed on these patients were cited as potential causes for an increase in plasma catecholamine concentration. Therefore, a 1-hour rest period was instituted before pneumoperitoneum to mitigate the expected effects of surgical stimulation (15). Mikami et al (15) saw no significantly increased catecholamine concentrations at a lower intraabdominal pressure of 10 mmHg.

These porcine model studies elucidated the effects of the type of insufflation gas and degree of intraabdominal pressure on the patient. This evidence suggested capnoperitoneum to have a profound metabolic and hemodynamic effect, as the various control groups using N2O, air, or helium insufflation did not experience any significant alterations in arterial PCO2 or pulmonary excretion of CO2 (11–15). Insufflation pressure likely contributes to these changes and is presumably related to the hemodynamic status of the patient, as even a small degree of vessel collapse can reduce blood flow by a substantial margin (15).

Intracranial hypertension

The effect of abdominal insufflation on intracranial pressure was assessed by Josephs et al (16) and Este-McDonald et al (17) who revealed significant increases in mean intracranial pressure with capnoperitoneum alone in 5 pigs undergoing laparoscopy in a reverse Trendelenburg position (16,17). Intracranial pressure was measured with an invasive probe placed within the left parietal cortex, and a balloon catheter was inserted into the epidural space over the right parietal cortex (16,17). Mean arterial blood pressure assessment, arterial pH measurements, and arterial blood gas analysis were performed at various times throughout the study (16,17). The intracranial pressure of the patient was artificially increased through inflation of an epidural balloon to simulate the effects of a head injury, and pneumoperitoneum appeared to exacerbate the increased intracranial pressure further by a significant margin, independent of arterial acid-base status or arterial PCO2 (16,17). Although acidemia and vasodilation mediated increases in cerebral blood flow were purported to be metabolic reasons for increased intracranial pressure, PCO2 and pH were not significantly different after the epidural balloon was inflated. Capnoperitoneum was shown to further exacerbate intracranial hypertension (16,17). The modified Monro-Kellie doctrine was cited, stating that a change in 1 intracranial compartment (cerebrospinal fluid, osseous, parenchymal, and vascular) leads to a reciprocal change in another non-osseous compartment (16,17). Josephs et al (16) and Este-McDonald et al (17) suggested intraabdominal pressure decreases outflow from the lumbar venous plexus, resulting in distension of the continuous vasculature within the spine and intracranial space. Due to the non-compliance of the osseous compartment, this results in an increased intracranial pressure (16,17). This mechanism is corroborated with other evidence, such as the documented intracranial hypertension associated with coughing, vomiting, or defecation, all of which increase intraabdominal pressure (16,17). Josephs et al (16) and Este-McDonald et al (17) performed a follow-up study in these patients using apneumatic retractors which did not result in the same intracranial hypertension, lending more evidence to the role of pneumoperitoneum in this process.

Another porcine study by Halverson et al (18) evaluated impaired lumbar venous drainage as the primary mechanism responsible for increased intracranial pressure and suggested this could be further exacerbated by patient positioning. Intracranial hypertension worsened with each 5-mmHg interval increase in intraabdominal pressure secondary to insufflation, independent of any changes in pH, mean arterial blood pressure, or arterial partial pressure of oxygen (PO2) and PCO2 (18). Patient placement into the Trendelenburg position further exacerbated intracranial hypertension and placement into the reverse Trendelenburg position was not shown to reduce this change in intracranial pressure (18). Halverson et al (18) also documented the positive correlation between lumbar spinal pressure, inferior vena cava pressure and intracranial pressure, lending further credence to the importance of the modified Monro-Kellie doctrine in the evaluation of intracranial hypertension secondary to this mechanism.

Although intracranial pressure can be measured via intraparenchymal probes or intraventricular catheterization, these techniques are not routinely employed in veterinary medicine due to their invasiveness and the associated complications including hemorrhage and infection (19,20). There is a substantial need for a non-invasive monitor of intracranial pressure in veterinary patients to provide more targeted, appropriate treatment and guide further diagnostic testing.

Optic nerve sheath diameter

Ultrasonographic measurement of the ONSD has been investigated as a surrogate measure of intracranial pressure to bypass the need for placement of an invasive monitor and provide rapid results with point-of-care, widely accessible equipment (20). As the optic nerve sheath is continuous with the dura mater, the space within the sheath is effectively an extension of subarachnoid space (20). Due to the noncompliant nature of the intracranial space, increases in intracranial pressure leads to compression of the cerebrospinal fluid compartment per the modified Monro-Kellie doctrine (16–18,20). The optic nerve sheath represents the path of least resistance for the pressurized cerebrospinal fluid, leading to distension of the sheath behind the globe that can be visualized ultrasonographically (20). In the evaluation of 65 humans with intracranial pathology at risk for intracranial hypertension, a cut-off ONSD value of 4.8 mm was used to identify an intracranial pressure of > 20 mmHg with a sensitivity of 96% and a specificity of 94% (20). The sensitivity dropped to 67% when the cut-off ONSD value was increased to 5.2 mm, demonstrating the need for caution in the interpretation of these values and the need for an appropriate cut-off, about false negative diagnoses, depending on the cut-off values used (20).

Optic nerve sheath diameter has been extensively explored in humans over the past decade and has been shown to be a reliable measure of intracranial pressure in multiple meta-analyses (21,22). In their systematic review of 12 other studies from years 1994 to 2012, Ohle et al (21) demonstrated that ultrasonographic evaluation of the ONSD showed good diagnostic test accuracy in comparison to CT. The reliability of ONSD measurements was further strengthened in a study by Robba et al (22) several years later. Ohle et al (21) noted the degree of innate variation in the fibrous trabecular network connecting the optic nerve sheath to the optic nerve and suggested this may be the underlying reason for the minor variability in sensitivity and specificity that had been noted thus far. Distension of the optic nerve sheath is dependent upon the strength of this network, which appears to vary among individuals and along the length of the sheath within any given individual (21). The location along the optic nerve sheath 3 mm behind the globe has been reported to be the point of maximal distension in humans and has been routinely used as a standardized location for obtaining ONSD measurements; but concern remains about variability among individuals (21,23).

Individual variation in ONSD was further explored in a recent article by Cardim et al (23), who evaluated healthy patients and those with intracranial hypertension confirmed with invasive monitoring devices. Cardim et al (23) stratified the population using a binary definition of sex (male and female) and age (young adult, adult, old adult) and measured ONSD 3 mm behind the globe, ultimately concluding that sex and age did not significantly influence ONSD measurements in patients with intracranial hypertension secondary to traumatic brain injuries. However, in the healthy population, ONSD was shown to be increased in both the elderly population and in males (23). There is a wide variety of conflicting evidence as to whether body mass index, ethnicity, age, sex, or other unknown factors can influence ONSD in humans (23). Further research will be required to determine whether different cut-off values for ONSD are required in humans that are more specific to the patient according to the aforementioned characteristics (23).

Discussion

In dogs, the measurement of ONSD has been shown to be accurate with no significant difference between this method and direct caliper measurement performed post-mortem (24). Lee et al (24) examined 15 dogs of 2 different breeds, and saw no correlation regarding age, sex, or body weight; but the ONSD measurements were significantly different among breeds. The results of this study are inherently limited by the small sample size but suggests different cut-off values may be necessary for different breeds in the diagnosis of intracranial pressure (24).

Ilie et al (8) evaluated the ONSD in 6 young healthy dogs in response to iatrogenically induced intracranial hypertension, measuring at a distance of 5 mm behind the globe and at the point of maximal distension, and demonstrated a nonlinear positive association between intracranial pressure and ONSD, especially at less than 20 mmHg above the established baseline (8). This is likely attributable to the physical capacity for distension as the sheath has a variable degree of elasticity and will not be distended beyond a certain degree (8). Ilie et al (8) induced intracranial hypertension with administration of anticoagulated autologous blood into the brain parenchyma and measured intracranial pressure with an invasive monitoring system. However, it is not known how different mechanisms of raised intracranial pressure affect the ONSD and there does not appear to be a firmly established gold standard for the monitoring of intracranial pressure in veterinary medicine, as this is not routinely used in practice (8).

Smith et al (25) attempted to characterize a reference range for the ultrasonographic evaluation of ONSD in 78 healthy adult dogs, and demonstrated that although OSND was associated with weight, age, and body condition score; much of the variance in this model was due to weight alone. Scrivani et al (26) previously evaluated canine ONSD with T2-weighted magnetic resonance imaging and established an association between body weight and ONSD. Smith et al (25) created an allometric model based on weight alone, which was able to accurately predict the ultrasonographically measured ONSD within 0.21 mm. Importantly, the mean interobserver differences in this study and other research in multiple species have been very low, suggesting this to be a consistent and reliable measurement (25–27). Although Smith et al (25) demonstrated a correlation in dogs between weight and ONSD, this association was not seen in equine or feline patients and may be species-specific (27,28).

More recently, Bramski et al (29) attempted to characterize an association between the direct measurement of intracranial pressure and the ultrasonographic measurement of the ONSD. In a population of 8 healthy horses under general anesthesia, intracranial pressure was measured directly with surgical placement of a transducer and ONSD was measured as the horses’ head positions were altered (29). Although some weak associations were observed, no strong consistent association was reported between intracranial pressure and ONSD with head position alterations in the equine model (29). The authors reported xylazine administration as a potential confounding factor (29). The administration of an alpha-2 adrenergic agonist may confound the proposed association between intracranial pressure and ONSD distension, as dexmedetomidine has been shown to partially attenuate the changes in ONSD in humans (30,31). Anesthetic considerations should be prioritized in any study attempting to evaluate ONSD as a surrogate measure of intracranial pressure.

There is a plethora of new literature regarding the measurement of ONSD in humans undergoing robot-assisted laparoscopic prostatectomies (RALP), a minimally invasive procedure requiring both capnoperitoneum and steep Trendelenburg positioning. Although the full implications of this research are beyond the scope of this review, it provokes further discussion regarding the impact of CO2 insufflation and patient positioning on intracranial pressure, as previously discussed by Halverson et al (18). Multiple sources demonstrate these conditions lead to an increased ONSD that is suggestive of intracranial hypertension, but 2 other studies offer conflicting results (32–37). A systematic review of this information by Kim et al (38) concluded that intracranial hypertension can be predicted by increases in ONSD throughout capnoperitoneum, but further research is required to determine the effect of other confounding factors that may influence these results. Recent investigation into the effects of various anesthetic agents suggest a myriad of factors are likely underlying this complex mechanism. Dexmedetomidine, propofol, and mannitol have all been shown to attenuate the increase in ONSD throughout laparoscopic procedures (30,31,39–41). Although this might suggest potential utility in the protection and maintenance of adequate cerebral perfusion pressure, the effect of these anesthetic agents on ONSD should be noted as they are routinely used in veterinary medicine as well.

Other anesthetic considerations include the maintenance of end-tidal carbon dioxide partial pressure (ETCO2) in the evaluation of optic nerve sheath diameter. An elevation in arterial PCO2 as measured via ETCO2 results in increased cerebral blood flow. This increased cerebral blood flow further contributes to the exertion of pressure upon the other non-osseous compartments within the calvarium, per the previously discussed Monro-Kellie doctrine, resulting in an increased ONSD (16,17). As there are multiple mechanisms associated with increased intracranial pressure secondary to laparoscopic insufflation, the standardization of ETCO2 is critical in the evaluation of ONSD.

In conclusion, it is currently unknown whether laparoscopy and capnoperitoneum lead to increased intracranial pressure in dogs. Previous research has demonstrated the effects of laparoscopy and capnoperitoneum on intracranial pressure in humans, but this information remains largely uncharacterized in veterinary medicine. Intracranial hypertension could represent an underrecognized or unknown complication of laparoscopic procedures, and as minimally invasive surgery becomes more common in unhealthy patients, it will be important to understand all of the associated risks in patients presenting with comorbidities. Patient selection remains crucial to the overall success of laparoscopic procedures, and further research in this area could help guide clinicians in this process.

Optic nerve sheath diameter has been used as an indirect measure of intracranial pressure in multiple species, and the reliability of this measurement has been specifically demonstrated in dogs. Examining the effects of laparoscopy on intracranial pressure as measured by ONSD in a healthy group of dogs represents a research opportunity that could have a profound effect on anesthetic considerations and surgical planning in veterinary medicine. CVJ

Footnotes

Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office (hbroughton@cvma-acmv.org) for additional copies or permission to use this material elsewhere.

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