Minimally invasive surgery with endoscopic techniques has been gaining popularity in companion animal medicine.1–4 Laparoscopic approaches for canine and feline patients for routine and complex surgical procedures are well described.2,5–9 Minimally invasive surgical procedures modified for use in some exotic small mammals, particularly domestic rabbits, have also been described.4,10–12 Laboratory rabbits have also been used in research for pediatric laparoscopic surgical techniques.13,14 Despite the widespread use of laparoscopy in rabbits, the veterinary medical literature is lacking a detailed assessment of optimal IAPs for use in this species.
When creating pneumoperitoneum for laparoscopic surgery, it is critical to understand which IAP will provide the greatest increase in working space while minimizing adverse effects on cardiorespiratory function and local tissue perfusion.15–18 Working space refers to the volume of abdominal space created by insufflation to allow for visual access and instrument handling during laparoscopic procedures. It is dependent on fixed factors (eg, patient size, gastrointestinal contents, and presence of organomegaly) as well as factors that can be adjusted (eg, IAP, patient ventilation, and muscle tone effects of the anesthetic protocol).19 These factors need to be taken into account when evaluating the effect of a variable such as IAP on the working space.
Working space has been investigated in pigs and cats,19,20 but to the authors’ knowledge, there are currently no recommendations for optimal working space in rabbits. In 1 study,20 working space in cats was assessed by changes in abdominal width, height, and circumference at various IAPs. Significant increases in abdominal circumference were identified with IAP increases from 4 to 8 mm Hg and from 8 to 15 mm Hg.20 Nevertheless, the authors concluded that an IAP of 15 mm Hg, compared with 8 mm Hg, did not provide a sufficient clinically important difference in working space to justify its use and found that the higher pressure was associated with increased mean arterial blood pressure and Paco2. A study19 of pigs used CT to measure the intra-abdominal volume at pressures of 0, 5, 10, and 15 mm Hg.19 The CT-measured volume increased by approximately 93% between pressures of 5 and 10 mm Hg and by approximately 19% between pressures of 10 and 15 mm Hg; therefore, the increase in working space in pigs was deemed beneficial with an increase in IAP up to, but not beyond, 10 mm Hg.
The objective of the study reported here was to evaluate the effect of changes in IAP (from 4 to 12 mm Hg) created with CO2 insufflation on the working space in rabbits as assessed by measurement with abdominal CT. These pressures were selected in accordance with recommendations for other companion animal species, as well as previous reports that described laparoscopic procedures used in rabbits.4,10–12 On the basis of the previously described studies in cats and pigs,19,20 we hypothesized that the working space for laparoscopic procedures would increase with increases in IAP, although not necessarily in a linear manner.
Materials and Methods
Animals
On the basis of sample size calculation (α = 0.05; β = 0.2; Cohen d = 1.4), 6 specific pathogen–free female New Zealand White rabbits (Oryctolagus cuniculus) obtained from a commercial sourcea were used in the study. The median body weight was 3.39 kg (range, 3.19 to 3.6 kg), and all rabbits were 4 to 5 months of age. The rabbits underwent physical examination prior to general anesthesia and were deemed healthy, except that 1 rabbit was found to have a heart murmur, which was identified on echocardiographic examination as being caused by tricuspid dysplasia. This was not considered likely to affect abdominal volume with insufflation, and the rabbit was not excluded from the study. The study protocol was reviewed and approved by the Animal Care Committee of the University of Guelph in accordance with guidelines set by the Canadian Council on Animal Care.
Anesthesia
Food was withheld from the rabbits for 1.5 to 2.5 hours prior to premedication. Midazolamb (1 mg/kg) and buprenorphine hydrochloridec (0.05 mg/kg) were administered IM. After 15 minutes, a 22-gauge IV catheterd was placed in a lateral auricular vein and crystalloid fluidse were administered IV during the anesthetic procedure at 5 mL/kg/h. Propofolf (8 to 11 mg/kg) was administered IV to induce anesthesia. The rabbits were intubated with 4-mm uncuffed endotracheal tubes by use of an over-the-endoscope technique and were connected to non-rebreathing Bain circuits delivering isofluraneg at concentrations of 2.5% to 3.5% in oxygen to maintain anesthesia. Manual intermittent positive-pressure ventilation was used to maintain Petco2 < 50 mm Hg, as measured by microstream capnography,h when the rabbits were not breathing spontaneously. The Petco2, oxygen saturation as measured by pulse oximetry,i heart rate as measured by an ultrasonic Doppler probe,j respiratory rate, and rectal temperature were monitored during anesthesia. Temperature was intermittently measured with a digital thermometer, and warming was provided as needed by use of a forced-air system.k
Experimental procedure
A balanced crossover design was used for the following IAPs: 4, 8, and 12 mm Hg. The pressures were ordered into 6 distinct random sequences with two 3-by-3 Latin squares generated by use of statistical software.l The 6 rabbits were randomly assigned to an IAP sequence with the same software.l
Each rabbit was placed in dorsal recumbency on the CT table, and a 16-slice CT scanm of the abdomen and thorax (slice thickness, 0.625 mm; 120 kVp; 140 mA) was performed to obtain baseline data prior to cannula placement. The pitch was 0.938:1, and rotation time was 1 second. After cannula placement, IAPs were created with a mechanical CO2 insufflatorn according to the sequence assigned to each rabbit. Additional CT scans were performed after the assigned pressure was maintained for ≥ 15 minutes. Propofol (1.5 to 3 mg/kg) was administered as needed to slow respiratory rates or induce apnea for the scans. Scans were performed with each rabbit in dorsal, left lateral oblique, and right lateral oblique recumbency with wedges placed to achieve an approximate 45° angle of the dorsoventral axis to the table surface. Cranially and caudally oriented endoscopic intra-abdominal images were recorded at each pressure by use of a 2.7-mm sheathed rigid endoscopeo for subjective visual assessment of laparoscopic working space. After CT scans were performed, the abdomen was purged of CO2 for 5 minutes prior to insufflating to the next IAP in the assigned sequence. After all scans, the abdomen was purged of CO2, the cannula was removed, and the linea alba and skin were apposed with 4–0 polydioxanone suturep in simple interrupted and continuous intradermal patterns, respectively.
Cannula placement
The ventral portion of the abdomen was routinely clipped of fur and aseptically prepared. Abdominal access was gained with a modified Hasson technique. Briefly, a skin incision was made immediately caudal to the umbilicus with a No. 15 scalpel blade. Subcutaneous fat was bluntly dissected, and stay sutures of 4–0 polydioxanonep were placed in the body wall on either side of the linea alba. The stay sutures were used to lift the body wall, and a small incision was made with a No. 15 scalpel blade prior to inserting a 5-mm plastic cannula with a blunted trocarq into the abdomen. Plastic cannulas were used to minimize artifacts during CT scanning. A 2.7-mm sheathed rigid endoscopeo was briefly passed through the cannula to ensure appropriate placement into the abdomen.
Postanesthetic management
Meloxicamr (1 mg/kg, SC) was administered to all rabbits prior to recovery from anesthesia. Flumazenilb (0.025 mg/kg; half of the volume IV and half SC) was administered to partially reverse the sedative effects of midazolam. Buprenorphine (0.05 mg/kg, SC) was administered 8 to 9 hours after the initial premedication dose. Intravenous catheters were removed prior to returning the rabbits to their housing facility. Vital signs were assessed twice daily for 3 days after anesthesia to ensure appropriate recovery. Meloxicams (1 mg/kg, PO, q 24 h) and buprenorphine (0.05 mg/kg, SC) were provided for analgesia on an individual basis as deemed necessary.
Working space calculation
A 3-D medical segmentation program and imaging software programt,u were used to convert DICOM-formatted CT images into 3-D models with the pneumoperitoneal gas isolated from abdominal viscera and gastrointestinal gas (Figure 1). The pneumoperitoneal gas was segmented with settings from a low of −1,024 HU to a high of −910 HU. Laparoscopic working space volumes were then calculated in cubic millimeters, which were converted to liters. These measurements were determined by an individual trained in use of the software and blinded to the IAPs used for each image captured.
Representative CT images (transverse view obtained at the level of the left kidney) depicting the difference in pneumoperitoneal (laparoscopic working space) volume in a domestic rabbit (Oryctolagus cuniculus) in dorsal recumbency at IAPs of 4 mm Hg (A), 8 mm Hg (B), and 12 mm Hg (C); a CT image of pneumoperitoneal gas isolated from gas within the gastrointestinal tract by use of medical imaging software (D); and a 3-D image of working space volume created by the combination of contiguous transverse CT sections (E) after CO2 insufflation.
Citation: American Journal of Veterinary Research 81, 1; 10.2460/ajvr.81.1.77
Statistical analysis
Data were analyzed with statistical software.l A mixed linear regression model was created with working space volume as the outcome measure; rabbit identification number was a random effect in the crossover design study, and pressure order, position (dorsal vs right or left lateral oblique recumbency), and IAP were fixed effects. Residual plots were used to assess linearity, homoscedasticity, and normality of residuals and to visually examine the data for outliers. Quantile plots of the residuals were also used to assess normality. All assumptions of linear mixed models were verified for the fitted model. The fixed effect variable of rabbit position did not improve the fit of the model on the basis of Akaike Information Criterion and was therefore removed from the final model. A type III ANOVA was performed on the fixed effects, and post hoc comparisons were performed with a Tukey adjustment. Values of P < 0.05 were considered significant. Figures were created with a data visualization package of the statistical software.21
Results
Positioning of rabbits (dorsal vs left or right lateral oblique recumbency) did not significantly (P = 0.357) affect the laparoscopic working space volume (Figure 2). A significant (P < 0.001) interaction effect was detected between treatment order (ie, the order of the 3 different IAPs used in the model) and IAP (Figure 3). This effect could not be interpreted in any meaningful manner when comparing individual means; however, the following results were reported from the model including the interaction term. There was a significant (P < 0.001) effect of IAP on working space volume. The working space volumes achieved at each IAP are reported (Table 1); mean working space volume was 19% greater with an IAP of 8 mm Hg, compared with 4 mm Hg (P < 0.001) and was 6.9% greater with an IAP of 12 mm Hg, compared with 8 mm Hg (P < 0.001). The order of treatment also had a significant (P < 0.001) effect on working space volume. For an IAP of 4 mm Hg, working space volume was lower when applied first in the order rather than when applied second or third. For an IAP of 8 mm Hg, a difference in volume was found when applied second, compared with third, in the sequence; however, the volume did not sequentially increase with increasing order. Representative CT (Figure 1) and endoscopic images (Figure 4) were used to depict the working space available with the 3 experimental IAPs.
Mean ± SD pneumoperitoneal (laparoscopic working space) volume in 6 domest ic rabbits with IAPs of 4, 8, and 12 mm Hg established by CO2 insufflation and imaged in various positions. Measurements of working space for anesthetized rabbits in dorsal (circles), left lateral oblique (triangles), and right lateral oblique (squares) recumbency were made from CT images and converted into 3-D models with medical imaging software; volumes calculated in cubic millimeters were converted to liters for reporting. The positioning of rabbits did not significantly affect working space volume.
Citation: American Journal of Veterinary Research 81, 1; 10.2460/ajvr.81.1.77
Measurements of mean ± SD laparoscopic working space volume for the 6 rabbits in Figure 2 at IAPs of 4, 8, and 12 mm Hg (circles, triangles, and squares, respectively) depicting the influence of treatment order (ie, the sequence in which each IAP was created in a given rabbit). There was a significant (P < 0.001) interaction effect between treatment order and IAP.
Citation: American Journal of Veterinary Research 81, 1; 10.2460/ajvr.81.1.77
Measurement of pneumoperitoneal (laparoscopic working space) volume in 6 anesthetized domestic rabbits (Oryctolagus cuniculus) with IAPs of 4, 8, and 12 mm Hg established by CO insufflation.
| Volume (L) | ||
|---|---|---|
| IAP (mm Hg) | Mean ± SD | Range |
| 4 | 0.825 ± 0.157a | 0.644–1.080 |
| 8 | 0.982 ± 0.168b | 0.801–1.277 |
| 12 | 1.050 ± 0.177c | 0.853–1.341 |
Volumes with different superscript letters differ significantly (P < 0.001).
Representative caudocranial (A, B, and C) and craniocaudal (D, E, and F) endoscopic images from a subset of the 6 rabbits in Figure 2 obtained during evaluation of working space achieved by CO2 insufflation to IAPs of 4 (A and D), 8 (B and E), and 12 (C and F) mm Hg. The diaphragm (black arrowhead), liver (white arrowhead), small intestine (chevron), and cecum (asterisk) are seen. The images allow a subjective assessment of working space available for laparoscopic procedures.
Citation: American Journal of Veterinary Research 81, 1; 10.2460/ajvr.81.1.77
Adverse effects were detected with pneumoperitoneum in rabbits and were in some cases more apparent at higher IAPs. After insufflation to 8 or 12 mm Hg, apnea in all rabbits and increased Petco2 (50 to 60 mm Hg) in 5 of 6 rabbits necessitated the use of higher positive-pressure ventilation rates. Subjectively increased heart rate (> 200 beats/min vs 160 to 200 beats/min at baseline) was noted at 8 and 12 mm Hg in 1 rabbit. One rabbit developed subcutaneous emphysema as a result of inappropriate cannula placement and was given meloxicam and buprenorphine at the previously described dosages for 2 days after the surgery. A second rabbit had signs of gastrointestinal discomfort after the anesthetic event (ie, increased intestinal gas, tense response on abdominal palpation, anxious behavior, and hyperthermia). This animal also received additional meloxicam and buprenorphine for 2 days. All other rabbits recovered uneventfully from the anesthesia and abdominal insufflation.
Discussion
Current recommendations for IAPs to be used during laparoscopic surgeries in species other than rabbits range from 6 to 10 mm Hg.22 For dogs, an IAP of 8 to 12 mm Hg is considered to have minimal effects on hemodynamic variables.23 Investigators of a study20 of induced pneumoperitoneum in cats concluded that pressures of 4 and 8 mm Hg provided adequate visual access for abdominal organs and that an IAP > 8 mm Hg may not yield clinically relevant improvements in working space. Successful laparoscopic ovariectomy was performed in cats when IAPs of 4 mm Hg9 and 6 mm Hg24 were created. In the authors’ experiences, however, lower IAPs can result in less abdominal wall tension, leading to increased movement and compression of the abdominal wall during certain laparoscopic surgeries.25 Abdominal wall tension can be considered in future studies together with measurements of working space to aid in the selection of optimal IAP for laparoscopic procedures in rabbits.
The effect of IAP on laparoscopic working space volumes in pigs has been evaluated by CT.19,26,27 The working space volume was found to increase by 93% with an increase in IAP from 5 to 10 mm Hg and by 19% with an increase in IAP from 10 to 15 mm Hg in 20-kg adult pigs.19 In that study,19 the volume expansion was attributed to a significant increase in the ventrodorsal distance (the maximum diameter from the ventral aspect of the abdominal wall to the ventral aspect of the vertebrae) and the maximal craniocaudal length of the abdomen (from pubis to diaphragm); there was no significant change in the internal width of the abdomen. A similar study26 in 6-kg juvenile pigs found the same effect, with a linear increase in working space volume as IAP increased from 0 to 8 mm Hg, followed by a decline in abdominal wall compliance with IAPs > 8 mm Hg. Interestingly, it was also found that prestretching of the abdominal wall, achieved by applying higher IAP and then desufflating the abdomen, allowed for a significant increase in working space volume at each IAP examined.26,27 This is an important area for future investigation of pneumoperitoneum in rabbits, as prestretching might allow for greater working space without use of a high IAP during the procedure.
The exact working space volume required for a laparoscopic procedure will depend on the organs being accessed and the instruments used; however, there may not be a meaningful increase in working space volume with IAPs > 8 mm Hg. A significantly larger working space was identified for rabbits in the present study at an IAP of 12 mm Hg than at an IAP of 8 mm Hg. Nevertheless, as was described in experiments involving pigs,19 the increase in volume with increased IAP in rabbits was not linear, and the percentage difference was much smaller between 8 and 12 mm Hg (6.9%) than between 4 and 8 mm Hg (19%). This was likely a result of abdominal wall biomechanical properties, as previously described with the creation of pneumoperitoneum in human patients.28 By increasing the IAP from 0 to 12 mm Hg in people, approximately 90% of the working space volume at 12 mm Hg is achieved by the time the IAP reaches 4 mm Hg.28 Therefore, it has been suggested that abdominal working space can be optimized at lower IAPs than traditionally used. This may be even more applicable during prolonged laparoscopic procedures when the hemodynamic and respiratory effects of CO2 insufflation become of greater concern for the patient.
For the present crossover study, each rabbit had the 3 IAPs applied in a randomly assigned sequence. The order of these treatments had a significant effect on working space volume, especially at 4 mm Hg. This effect may have been attributable to the prestretching phenomenon previously described.27 When the IAP of 4 mm Hg was applied first in the sequence, no prior stretching had occurred. When applied following higher pressures (8 and 12 mm Hg), the working space volume achieved appeared to be greater. Interestingly, the effect differed when assessing the influence of treatment order on working space volume at 8 mm Hg; a significant difference in working space was detected when this IAP was applied second or third in the sequence, compared with that achieved when it was used first, but the working space did not sequentially increase with each pressure as observed at 4 mm Hg. The inability to detect a consistent effect at an IAP of 8 and 12 mm Hg may have been attributable to a lack of power, considering the small number of rabbits used in this study. For each IAP in each treatment order position (first, second, or third), there were only 2 observations from which to draw conclusions. It was also possible that the observed interaction effects resulted from washout (desufflation) periods that were too short. As our design was balanced for carryover effects, these effects were considered unlikely to confound our results. An interaction between order and IAP existed, and we recommend that future studies on working space randomize and account for the effect of sequence on the entire model. Randomization of crossover studies requires a balanced Latin square design to control for carryover effects, which can also be assessed in the statistical model.
As mentioned, a small sample size was the main limitation of this study. To limit the influence of individual animal effects on variability in working space volumes, the rabbits used in the study were of the same breed and similar in size and age, and a crossover design was used to ensure that each rabbit served as its own control for comparison among IAPs. No significant outliers were found in the assessment of data for individual rabbits. In a priori calculations, the sample size was deemed appropriate to identify differences in working space volume associated with different IAPs; however, evaluating the interaction effect with treatment order may require a larger sample.
The adverse effects observed in these rabbits have been previously reported for other species with pneumoperitoneum created to facilitate laparoscopic procedures.17,29 Apnea is expected to be secondary to pressure on the thorax, decreased thoracic compliance, and difficulty in spontaneous ventilation. End-tidal partial pressures of CO2 are commonly increased with pneumoperitoneum owing to decreases in venous return and cardiac output as well as absorption of insufflated CO2 across the peritoneal wall. Increased heart rate is expected to result from increases in Paco2 that cause sympathetic stimulation, and this change in heart rate may help to maintain cardiac output. These cardiovascular and respiratory effects did not seem to be a clinically important concern in this population of healthy young rabbits. Nevertheless, adverse effects associated with pneumoperitoneum created by CO2 insufflation need to be evaluated with further studies in rabbits.
Emphysema and postanesthetic gastrointestinal effects were each reported for 1 rabbit in the present study. Emphysema is a known adverse effect that can result from inappropriate cannula placement during induction of pneumoperitoneum.30,31 Gastrointestinal signs in 1 rabbit may have resulted from effects of anesthesia32,33 or changes in splanchnic circulation during pneumoperitoneum, as summarized in a systematic review34 that included studies of animals. Our results suggested that, depending on the visibility needed and instruments required for a specific laparoscopic procedure, it may not be advantageous to use an IAP > 8 mm Hg in rabbits. This information can be used in further research to develop guidelines for pneumoperitoneum use during minimally invasive surgery in rabbits.
Acknowledgments
Supported by the Ontario Veterinary College Pet Trust. The funding agency did not contribute to the design, data collection, analysis, or writing of this manuscript.
The authors declare that there were no conflicts of interest.
The authors thank John Phillips for assistance and expertise in use of 3-D imaging software to determine pneumoperitoneal volumes.
ABBREVIATIONS
| Petco2 | End-tidal partial pressure of CO2 |
| IAP | Intra-abdominal pressure |
Footnotes
Charles River Laboratories, Saint-Constant, QC, Canada.
Sandoz Canada Inc, Boucherville, QC, Canada.
Vetergesic, Sogeval UK Ltd, Sheriff Hutton, England.
BD Canada, Mississauga, ON, Canada.
Plasmalyte-A, Baxter Healthcare, Deerfield, Ill.
Pharmascience Inc, Montreal, QC, Canada.
IsoFlo, Zoetis Canada Inc, Kirkland, QC, Canada.
Nellcor, Covidien Canada, Saint-Laurent, QC, Canada.
2500A VET, Nonin Medical Inc, Plymouth, Minn.
Ultrasonic Doppler 811-B, Parks Medical Electronics Inc, Aloha, Ore.
Bair Hugger, 3M, London, ON, Canada.
R, version 3.4.1, R Core Team, R Foundation for Statistical Computing, Vienna, Austria.
GE Bright Speed, GE Healthcare, Milwaukee, Wis.
Stryker, Kalamazoo, Mich.
Karl Storz Endoscopy America Inc, El Segundo, Calif.
PDS II, Ethicon, Johnson & Johnson Medical Products, Markham, ON, Canada.
VersaOne, Covidien Canada, Saint-Laurent, QC, Canada.
Metacam, 20 mg/mL injectable, Boehringer Ingelheim, Burlington, ON, Canada.
Metacam, 1.5 mg/mL oral suspension, Boehringer Ingelheim, Burlington, ON, Canada.
Materialise Mimics, version 19, Materialise, Leuven, Belgium.
3-matic, version 11, Materialise, Leuven, Belgium.
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