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    Mean ± SD blood pH (A) and peritoneal fluid pH (B) for 9 dogs that had CO2 insufflation of the abdominal cavity for laparoscopic teaching procedures. Time points 1 to 4 represent (mean ± SD) 8.5 ± 3 minutes, 24.5 ± 5 minutes, 44.5 ± 7.0 minutes, and 72.0 ± 14 minutes after insufflation, respectively. *Value differs significantly (P < 0.05) from the value for time point 1.

  • 1.

    Barnes RF, Greenfield CL, Schaeffer DJ, et al. Comparison of biopsy samples obtained using standard endoscopic instruments and the harmonic scalpel during laparoscopic and laparoscopic-assisted surgery in normal dogs. Vet Surg 2006;35:243251.

    • Search Google Scholar
    • Export Citation
  • 2.

    Davidson EB, Moll HD, Payton ME. Comparison of laparoscopic ovariohysterectomy and ovariohysterectomy in dogs. Vet Surg 2004;33:6269.

  • 3.

    Rawlings CA, Mahaffey MB, Bement S, et al. Prospective evaluation of laparoscopic-assisted gastropexy in dogs susceptible to gastric dilatation. J Am Vet Med Assoc 2002;221:15761581.

    • Search Google Scholar
    • Export Citation
  • 4.

    Lew M, Jalynski M, Kasprowicz A, et al. Laparoscopic cryptorchidectomy in dogs—report of 15 cases. Pol J Vet Sci 2005;8:251254.

  • 5.

    Brisson BA, Reggeti F, Bienzle D. Portal site metastasis of invasive mesothelioma after diagnostic thoracoscopy in a dog. J Am Vet Med Assoc 2006;229:980983.

    • Search Google Scholar
    • Export Citation
  • 6.

    Meininger D, Byhahn C, Bueck M, et al. Effects of prolonged pneumoperitoneum on hemodynamics and acid-base balance during totally endoscopic robot-assisted radical prostatectomies. World J Surg 2002;26:14231427.

    • Search Google Scholar
    • Export Citation
  • 7.

    Cawich SO, Mitchell DI, Newnham MS, et al. A comparison of open and laparoscopic cholecystectomy done by a surgeon in training. West Indian Med J 2006;55:103109.

    • Search Google Scholar
    • Export Citation
  • 8.

    Hollingsworth JM, Miller DC, Dunn RL, et al. Cost trends for oncological renal surgery: support for a laparoscopic standard of care. J Urol 2006;176:10971101.

    • Search Google Scholar
    • Export Citation
  • 9.

    Curet MJ. Port site metastases. Am J Surg 2004;187:705712.

  • 10.

    Ramirez PT, Frumovitz M, Wolf JK, et al. Laparoscopic portsite metastases in patients with gynecological malignancies. Int J Gynecol Cancer 2004;14:10701077.

    • Search Google Scholar
    • Export Citation
  • 11.

    Mathew G, Watson DI, Rofe AM, et al. Wound metastases following laparoscopic and open surgery for abdominal cancer in a rat model. Br J Surg 1996;83:10871090.

    • Search Google Scholar
    • Export Citation
  • 12.

    Brundell SM, Tucker K, Texler M, et al. Variables in the spread of tumor cells to trocars and port sites during operative laparoscopy. Surg Endosc 2002;16:14131419.

    • Search Google Scholar
    • Export Citation
  • 13.

    Lee BR, Tan BJ, Smith AD. Laparoscopic port site metastases: incidence, risk factors, and potential preventive measures. Urology 2005;65:639644.

    • Search Google Scholar
    • Export Citation
  • 14.

    Wilkinson NW, Shapiro AJ, Harvey SB, et al. Port-site recurrence reproduced in the VX-2 rabbit carcinoma model: an in vivo model comparing laparoscopic port sites and open incisions. JSLS 2001;5:221226.

    • Search Google Scholar
    • Export Citation
  • 15.

    Ikramuddin S, Lucus J, Ellison EC, et al. Detection of aerosolized cells during carbon dioxide laparoscopy. J Gastrointest Surg 1998;2:580583.

    • Search Google Scholar
    • Export Citation
  • 16.

    Gamal EM, Szabo G, Nagy P, et al. The role of pneumoperitoneum and the “chimney effect” on the development of port site metastasis. A new experimental animal model using Furka's spleen tissue suspension. Magy Seb 2005;58:8992.

    • Search Google Scholar
    • Export Citation
  • 17.

    Neuhaus SJ, Watson DI, Ellis T, et al. The effect of immune enhancement and suppression on the development of laparoscopic port site metastases. Surg Endosc 2000;14:439443.

    • Search Google Scholar
    • Export Citation
  • 18.

    Burns JM, Matthews BD, Pollinger HS, et al. Effect of carbon dioxide pneumoperitoneum and wound closure technique on port site tumor implantation in a rat model. Surg Endosc 2005;19:441447.

    • Search Google Scholar
    • Export Citation
  • 19.

    Mathew G, Watson DI, Rofe AM, et al. Adverse impact of pneumoperitoneum on intraperitoneal implantation and growth of tumour cell suspension in an experimental model. Aust N Z J Surg 1997;67:289292.

    • Search Google Scholar
    • Export Citation
  • 20.

    Neuhaus SJ, Watson DI, Ellis T, et al. Influence of gases on intraperitoneal immunity during laparoscopy in tumor-bearing rats. World J Surg 2000;24:12271231.

    • Search Google Scholar
    • Export Citation
  • 21.

    Wildbrett P, Oh A, Naundorf D, et al. Impact of laparoscopic gases on peritoneal microenvironment and essential parameters of cell function. Surg Endosc 2003;17:7882.

    • Search Google Scholar
    • Export Citation
  • 22.

    Volz J, Koster S, Spacek Z, et al. Characteristic alterations of the peritoneum after carbon dioxide pneumoperitoneum. Surg Endosc 1999;13:611614.

    • Search Google Scholar
    • Export Citation
  • 23.

    Wong YT, Shah PC, Birkett DH, et al. Carbon dioxide pneumoperitoneum causes severe peritoneal acidosis, unaltered by heating, humidification, or bicarbonate in a porcine model. Surg Endosc 2004;18:14981503.

    • Search Google Scholar
    • Export Citation
  • 24.

    Monnet E, Twedt DC. Laparoscopy. Vet Clin North Am Small Anim Pract 2003;33:11471163.

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    Neuhaus SJ, Watson DI, Ellis T, et al. Metabolic and immunologic consequences of laparoscopy with helium or carbon dioxide insufflation: a randomized clinical study. Aust N Z J Surg 2001;71:447452.

    • Search Google Scholar
    • Export Citation
  • 26.

    Duke T, Steinacher SL, Remedios AM. Cardiopulmonary effects of using carbon dioxide for laparoscopic surgery in dogs. Vet Surg 1996;25:7782.

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    Fitzgerald SD, Andrus CH, Baudendistel LJ, et al. Hypercarbia during carbon dioxide pneumoperitoneum. Am J Surg 1992;163:186190.

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    Graham AJ, Jirsch DW, Barrington KJ, et al. Effects of intraabdominal CO2 insufflation in the piglet. J Pediatr Surg 1994;29:12761280.

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    Leighton T, Pianim N, Liu SY, et al. Effectors of hypercarbia during experimental pneumoperitoneum. Am Surg 1992;58:717721.

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    Neuhaus SJ, Watson DI. Pneumoperitoneum and peritoneal surface changes: a review. Surg Endosc 2004;18:13161322.

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    Farrell TM, Metreveli RE, Johnson AB, et al. Choice of insufflating gas influences on wound metastasis. Surg Endosc 2000;14:10471049.

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Changes in pH of peritoneal fluid associated with carbon dioxide insufflation during laparoscopic surgery in dogs

Felix M. Duerr Dr med vet1, David C. Twedt DVM2, and Eric Monnet DVM, PhD3
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  • 1 Department of Clinical Sciences, Veterinary Medical Center, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80523.
  • | 2 Department of Clinical Sciences, Veterinary Medical Center, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80523.
  • | 3 Department of Clinical Sciences, Veterinary Medical Center, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80523.

Abstract

Objective—To evaluate changes in pH of peritoneal fluid associated with CO2 insufflation during laparoscopy in dogs.

Animals—13 client-owned dogs and 10 purpose-bred teaching dogs.

Procedures—Laparotomy was performed on control dogs; peritoneal fluid pH was mea-sured at time of incision of the abdominal cavity (time 0) and 30 minutes later. Laparoscopic insufflation with CO2 was performed and routine laparoscopic procedures conducted on the teaching dogs. Insufflation pressure was limited to 12 mm Hg. Intraperitoneal fluid pH was measured by use of pH indicator paper at 4 time points. Arterial blood gas analysis was performed at the same time points.

Results—Peritoneal fluid pH did not change significantly between 0 and 30 minutes in the control dogs. For dogs with CO2 insufflation, measurements obtained were a mean of 8.5, 24.5, 44.5, and 72.0 minutes after insufflation. The pH of peritoneal fluid decreased signifi-cantly between the first (7.825 ± 0.350) and second (7.672 ± 0.366) time point. Blood pH decreased significantly between the first (7.343 ± 0.078), third (7.235 ± 0.042), and fourth (7.225 ± 0.038) time points. The PaCO2 increased significantly between the first (39.9 ± 9.8 mm Hg) and fourth (54.6 ± 4.4 mm Hg) time points. Base excess decreased significantly between the first and all subsequent time points.

Conclusions and Clinical Relevance—Pneumoperitoneum attributable to CO2 insufflation caused a mild and transient decrease in peritoneal fluid pH in dogs. Changes in peritoneal fluid associated with CO2 insufflation in dogs were similar to those in other animals.

Abstract

Objective—To evaluate changes in pH of peritoneal fluid associated with CO2 insufflation during laparoscopy in dogs.

Animals—13 client-owned dogs and 10 purpose-bred teaching dogs.

Procedures—Laparotomy was performed on control dogs; peritoneal fluid pH was mea-sured at time of incision of the abdominal cavity (time 0) and 30 minutes later. Laparoscopic insufflation with CO2 was performed and routine laparoscopic procedures conducted on the teaching dogs. Insufflation pressure was limited to 12 mm Hg. Intraperitoneal fluid pH was measured by use of pH indicator paper at 4 time points. Arterial blood gas analysis was performed at the same time points.

Results—Peritoneal fluid pH did not change significantly between 0 and 30 minutes in the control dogs. For dogs with CO2 insufflation, measurements obtained were a mean of 8.5, 24.5, 44.5, and 72.0 minutes after insufflation. The pH of peritoneal fluid decreased signifi-cantly between the first (7.825 ± 0.350) and second (7.672 ± 0.366) time point. Blood pH decreased significantly between the first (7.343 ± 0.078), third (7.235 ± 0.042), and fourth (7.225 ± 0.038) time points. The PaCO2 increased significantly between the first (39.9 ± 9.8 mm Hg) and fourth (54.6 ± 4.4 mm Hg) time points. Base excess decreased significantly between the first and all subsequent time points.

Conclusions and Clinical Relevance—Pneumoperitoneum attributable to CO2 insufflation caused a mild and transient decrease in peritoneal fluid pH in dogs. Changes in peritoneal fluid associated with CO2 insufflation in dogs were similar to those in other animals.

Laparoscopic techniques are being used with increasing frequency for a wide number of diagnostic and surgical procedures in veterinary medicine.1-5 In human medicine, laparoscopy is considered the standard technique for many surgical procedures.6-8 However, a major concern associated with laparoscopy for neoplastic disease in humans is port site metastasis,9-12 which is defined as early recurrent tumorous lesions that develop locally in the abdominal wall within the scar tissue of 1 or more trocar sites that are not associated with diffuse peritoneal carcinoma- tosis.13 Port site metastasis has only been reported in veterinary medicine after thoracoscopic surgery in a dog.5 Factors influencing port site metastasis are unknown9,12; however, direct contamination,14 aerosolization,15 the chimney effect,16 the local immune response,17 and establishment of pneumoperitoneum18 have been suggested as possible causes.

Studies11,19 in laboratory animals have revealed that CO2 insufflation increases the risk of tumor implantation. Other investigations into the effects of CO2-induced pneumoperitoneum revealed an association with intraperitoneal acidosis in rats,20,21 mice,22 and swine.23 Several investigators have proposed21,22 that alterations of the peritoneal surface as a result of intraperitoneal acidosis associated with CO2 insufflation may facilitate port site metastasis.

Laparoscopy is becoming a commonly used method for diagnostic and surgical procedures in dogs. Abdominal neoplasms in dogs are often biopsied by use of laparoscopy, but the risk for development of port site metastasis in these dogs is unknown. To our knowledge, alteration of intraperitoneal pH has not been investigated in dogs. The objective of the study reported here was to investigate the effect of CO2 insufflation on pH of intraperitoneal fluid in dogs. We hypothesized that CO2 insufflation during laparoscopy would not induce peritoneal fluid acidosis in dogs.

Materials and Methods

Animals—Thirteen client-owned female dogs undergoing routine ovariohysterectomy via a standard laparotomy technique were used as control dogs. Ten purpose-bred large-breed female dogs (approx body weight of each dog, 25 kg) used for a laparoscopy teaching course were the study population. All dogs were deemed healthy on the basis of results of a physical examination and no known history of disease. Clients provided written consent for use of their dogs in the study. The study protocol was approved by the Animal Care and Use Committee at Colorado State University.

Anesthesia—All dogs were anesthetized. A combination of 0.5 mg of acepromazine,a 25 mg of morphine,b and 0.5 mg of glycopyrrolateb was administered SC approximately 30 minutes prior to induction of anesthesia. Anesthesia was induced by IV administration of a combination of 150 mg of ketaminec and 7 mg of diazepam,d which allowed intubation of the trachea. Isofluranee in oxygen was administered to maintain a surgical plane of anesthesia. Lactated Ringer's solutionf was administered at an approximate rate of 5 mL/kg/h, IV, during surgery. Standard techniques (eye position, palpebral reflexes, and jaw tone) were used to evaluate anesthetic depth. Dogs were monitored continuously by use of ECG, direct blood pressure measurements, end-tidal capnography, and pulse oximetry. Positivepressure ventilation was not used in the control dogs but was used in all teaching dogs. Ventilator settings remained unchanged throughout the study period (tidal volume, approx 15 mL/kg; respiratory rate, 12 breaths/min; and inspiration:expiration ratio, approx 1:4). Dogs that became hypotensive (defined as mean arterial pressure < 60 mm Hg) were treated by IV admnistration of a bolus of crystalloid solution. Additional medications or treatments were used when necessary.

Control dogs—Laparotomy was performed on dogs in the control group. The pH was measured by use of a commercially available pH stripg (pH scale from 6.0 to 8.1) immediately after the abdominal cavity was incised (time 0) and approximately 30 minutes later before closure of the linea alba. A sterile cotton swab was used to collect abdominal fluid. The swab specimen was then applied to the nonsterile pH paper to measure peritoneal fluid pH. Measurements were determined by a single investigator. Blood gas analysis was not performed for the control group.

Teaching dogs with CO2 insufflation—Dogs were positioned in lateral or dorsal recumbency, and routine laparoscopic procedures (laparoscopic exploration of the abdominal cavity, collection of liver biopsy specimens, and ovariohysterectomy) were performed. Dogs were excluded when laparoscopic-assisted procedures that required deflation of the abdominal cavity were performed before completion of data acquisition.

A Veress needleh was used for insufflation of the abdominal cavity. Insufflation pressure was limited to 12 mm Hg. Time at which insufflation was completed (defined as abdominal distention at a pressure of 12 mm Hg without noticeable flow detection by the insufflating devicei) was recorded (time 0). Immediately after successful insufflation, routine placement of a laparoscopic cannula was performed as described else- where.24 This cannula was then used to obtain the first measurement of intraperitoneal fluid pH (time point 1). Measurements were repeated 3 additional times (time points 2, 3, and 4, respectively) at approximately 20minute intervals.

Peritoneal fluid pH was determined by cutting a small piece from a commercially available pH stripg such that the piece could be held with laparoscopic forceps. This was then inserted through an abdominal trocar and pressed against the abdominal wall. Care was taken to avoid obtaining a value from areas that contained blood. When severe blood contamination was detected, measurements were repeated. The pH strip was withdrawn from the abdominal cavity, and the pH was determined separately by 4 investigators. Values were determined by comparing the color of the pH strip to the pH scale provided by the manufacturer. All investigators were not aware of the dog or time point that served as the source of each sample. Arterial blood gas analysis was conducted at the same time points as the measurements of peritoneal fluid pH; samples were analyzed by use of a commercially available blood gas analyzer.j

Statistical analysis—For the peritoneal fluid pH in the dogs with CO2 insufflation, the lowest and highest value of each of the 4 measurements for a given time point were excluded from the analysis. The mean of the remaining 2 measurements was calculated. An ANOVA for repeated measurements was used to compare the value for the first pH measurement with values for each subsequent time point. Values of P < 0.05 were considered significant. Data were reported as mean ± SD.

Results

Control dogs—For the control group, mean ± SD pH was 8.03 ± 0.13 immediately after the abdominal cavity was incised. Thirty minutes later, mean pH was 8.08 ± 0.08. These values did not differ significantly (P = 0.298).

Teaching dogs with CO2 insufflation—The only complication detected for these dogs was hypotension during anesthesia in 4 dogs. Each of the 4 dogs received 1 or 2 fluid boluses of 100 mL of lactated Ringer's solution to treat hypotension. Two of the 4 dogs did not respond adequately to administration of the fluid boluses and therefore were administered 1 or 2 doses of ephedrinek (2.5 mg, IV), and 1 of these 2 dogs was subsequently treated by administration of dobutaminel as a continuous rate infusion (2 μg/kg/min, IV).

One dog was excluded because a laparoscopic-assisted procedure that required deflation of the abdominal cavity was performed prior to completion of data acquisition. Consequently, data were available for 9 dogs.

Measurements of peritoneal fluid pH were obtained at a mean ± SD of 8.5 ± 3 minutes, 24.5 ± 5 minutes, 44.5 ± 7 minutes, and 72.0 ± 14 minutes after insufflation for the first to fourth time points, respectively. Because of difficulty in obtaining blood samples close to the time at which pH of peritoneal fluid was measured, blood gas values were obtained for all 9 dogs at the first time point but only for 7, 6, and 8 dogs at the second, third, and fourth time points, respectively.

Peritoneal fluid pH decreased significantly (P = 0.020) between the first and second time points (Figure 1). Blood pH decreased significantly between the first time point and the third (P = 0.035) and fourth (P = 0.020) time points. The PaCO2 increased significantly (P = 0.002) between the first and fourth time points (Table 1). Base excess decreased significantly between the first time point and all subsequent time points. Bicarbonate concentrations did not differ significantly among any of the time points.

Table 1—

Mean ± SD values for blood gas analysis for 9 dogs that had CO2 insufflation of the abdominal cavity for laparoscopic teaching procedures.

Table 1—
Figure 1—
Figure 1—

Mean ± SD blood pH (A) and peritoneal fluid pH (B) for 9 dogs that had CO2 insufflation of the abdominal cavity for laparoscopic teaching procedures. Time points 1 to 4 represent (mean ± SD) 8.5 ± 3 minutes, 24.5 ± 5 minutes, 44.5 ± 7.0 minutes, and 72.0 ± 14 minutes after insufflation, respectively. *Value differs significantly (P < 0.05) from the value for time point 1.

Citation: American Journal of Veterinary Research 69, 2; 10.2460/ajvr.69.2.298

Discussion

Pneumoperitoneum attributable to insufflation with CO2 causes transient intraperitoneal acidosis in dogs. The findings for the study reported here are similar to those in other animals.20-23 However, in our study, a decrease in intraperitoneal pH was only detected during the initial period of CO2-induced pneumoperitoneum. This finding is consistent with results of a clinical study25 in humans undergoing laparoscopic surgery.

Changes in blood pH in our study population were comparable to those in a study26 in dogs in which investigators evaluated the cardiopulmonary effects of CO2 insufflation. No significant changes in PaCO2 were detected in that study because it had been designed to maintain a constant end-tidal CO2 throughout the procedure. In contrast, our study was designed to allow changes at a fixed ventilator setting that would be commonly used in practice. In the study reported here, intraperitoneal pH decreased significantly only within the first 20 minutes after insufflation and then stabilized. Those changes were likely caused by peritoneal fluid acidosis and carbonic acid production, rather than systemic hypercarbia and acidemia, because the blood pH, PaCO2, and base excess decreased over the entire study period.

Significant differences between sample time points for blood pH and PaCO2 were detected toward the end of the study period. In contrast, significant changes for peritoneal fluid pH were not evident at the conclusion of the study period. If the changes in peritoneal fluid pH were secondary to systemic changes, it would be expected that they would follow the same pattern of systemic alterations (ie, they should have changed toward the end of the study period). In a study25 in human patients, this finding was even more dramatic because peritoneal acidosis was only detected 10 minutes after insufflation, and there was a shift from the initial peritoneal acidosis toward alkalosis after 30 minutes of insufflation. The difference between results for that study25 and our results is more likely attributable to the application of positive-pressure ventilation. In other studies,27-29 investigators have reported that intra-abdominal insufflation with CO2 is associated with systemic hypercarbia and acidemia. These changes are attributable to systemic absorption of CO2.30 In the study reported here, changes in base excess were mild and were detected during the entire study period, which would make it unlikely that they were related to the peritoneal fluid changes.

Changes in pH of peritoneal fluid in the study reported here are consistent with results of other studies20,23 in which investigators found a decrease in intraperitoneal pH. These changes likely resulted from the direct effects of CO2 insufflation; however, they may also have been caused by impaired tissue perfusion secondary to abdominal insufflation.31 Regardless of the cause of intraperitoneal acidosis, concerns exist in human medicine with regard to the potential correlation with port site metastasis.

Several procedures to prevent changes in intraperitoneal pH have been investigated. Heating, humidification, and use of bicarbonate had a positive effect on peritoneal acidosis in 1 study23; however, that result was not statistically significant. Intraperitoneal lavage, gasless laparoscopy, and use of helium instead of CO2 have also been used with mixed results.20,25,32-35

A shortcoming of the study reported here was the lack of an exactly similar control group. In our control group, the technique used to measure intraperitoneal pH was not exactly the same as for the laparoscopic group; thus, we did not proceed with statistical comparison between the groups. It would have been beneficial to include a control group insufflated with an inert gas such as helium. However, special insufflators are needed for the administration of helium, and these insufflators were not available to the authors.

Analysis of the results of the study reported here established that pneumoperitoneum attributable to CO2 insufflation can lead to peritoneal fluid acidosis, at least at the onset of the insufflation period. Peritoneal fluid changes associated with CO2 insufflation in dogs are similar to those in humans and other animals. These changes may facilitate tumor implantation during laparoscopic surgery in cancer patients. Because dogs appear to have a response to CO2 insufflation that is similar to the response for human patients, dogs may be useful in studies conducted to investigate strategies to decrease the risk of port site metastasis.

a.

Vedco Inc, St Joseph, Mo.

b.

Baxter Healthcare Corp, Deerfield, Ill.

c.

VetaKet, Phoenix Scientific Inc, St Joseph, Mo.

d.

Hospira Inc, Lake Forest, Ill.

e.

Abbott Laboratories, North Chicago, Ill.

f.

Hospira Inc, Lake Forest, Ill.

g.

pH-indicator type CS, Whatman International Ltd, Maidstone, England.

h.

Auto Suture, United States Surgical Corp, Norwalk, Conn.

i.

Storz Endoflator 26012, Karl Storz Endovision, Charlton, Mass.

j.

IRMA Trupoint blood gas analysis system, ITC, Edison, NJ.

k.

Parenta Pharmaceuticals Inc, West Columbia, SC.

l.

Bedford Laboratories, Bedford, Ohio.

References

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    Barnes RF, Greenfield CL, Schaeffer DJ, et al. Comparison of biopsy samples obtained using standard endoscopic instruments and the harmonic scalpel during laparoscopic and laparoscopic-assisted surgery in normal dogs. Vet Surg 2006;35:243251.

    • Search Google Scholar
    • Export Citation
  • 2.

    Davidson EB, Moll HD, Payton ME. Comparison of laparoscopic ovariohysterectomy and ovariohysterectomy in dogs. Vet Surg 2004;33:6269.

  • 3.

    Rawlings CA, Mahaffey MB, Bement S, et al. Prospective evaluation of laparoscopic-assisted gastropexy in dogs susceptible to gastric dilatation. J Am Vet Med Assoc 2002;221:15761581.

    • Search Google Scholar
    • Export Citation
  • 4.

    Lew M, Jalynski M, Kasprowicz A, et al. Laparoscopic cryptorchidectomy in dogs—report of 15 cases. Pol J Vet Sci 2005;8:251254.

  • 5.

    Brisson BA, Reggeti F, Bienzle D. Portal site metastasis of invasive mesothelioma after diagnostic thoracoscopy in a dog. J Am Vet Med Assoc 2006;229:980983.

    • Search Google Scholar
    • Export Citation
  • 6.

    Meininger D, Byhahn C, Bueck M, et al. Effects of prolonged pneumoperitoneum on hemodynamics and acid-base balance during totally endoscopic robot-assisted radical prostatectomies. World J Surg 2002;26:14231427.

    • Search Google Scholar
    • Export Citation
  • 7.

    Cawich SO, Mitchell DI, Newnham MS, et al. A comparison of open and laparoscopic cholecystectomy done by a surgeon in training. West Indian Med J 2006;55:103109.

    • Search Google Scholar
    • Export Citation
  • 8.

    Hollingsworth JM, Miller DC, Dunn RL, et al. Cost trends for oncological renal surgery: support for a laparoscopic standard of care. J Urol 2006;176:10971101.

    • Search Google Scholar
    • Export Citation
  • 9.

    Curet MJ. Port site metastases. Am J Surg 2004;187:705712.

  • 10.

    Ramirez PT, Frumovitz M, Wolf JK, et al. Laparoscopic portsite metastases in patients with gynecological malignancies. Int J Gynecol Cancer 2004;14:10701077.

    • Search Google Scholar
    • Export Citation
  • 11.

    Mathew G, Watson DI, Rofe AM, et al. Wound metastases following laparoscopic and open surgery for abdominal cancer in a rat model. Br J Surg 1996;83:10871090.

    • Search Google Scholar
    • Export Citation
  • 12.

    Brundell SM, Tucker K, Texler M, et al. Variables in the spread of tumor cells to trocars and port sites during operative laparoscopy. Surg Endosc 2002;16:14131419.

    • Search Google Scholar
    • Export Citation
  • 13.

    Lee BR, Tan BJ, Smith AD. Laparoscopic port site metastases: incidence, risk factors, and potential preventive measures. Urology 2005;65:639644.

    • Search Google Scholar
    • Export Citation
  • 14.

    Wilkinson NW, Shapiro AJ, Harvey SB, et al. Port-site recurrence reproduced in the VX-2 rabbit carcinoma model: an in vivo model comparing laparoscopic port sites and open incisions. JSLS 2001;5:221226.

    • Search Google Scholar
    • Export Citation
  • 15.

    Ikramuddin S, Lucus J, Ellison EC, et al. Detection of aerosolized cells during carbon dioxide laparoscopy. J Gastrointest Surg 1998;2:580583.

    • Search Google Scholar
    • Export Citation
  • 16.

    Gamal EM, Szabo G, Nagy P, et al. The role of pneumoperitoneum and the “chimney effect” on the development of port site metastasis. A new experimental animal model using Furka's spleen tissue suspension. Magy Seb 2005;58:8992.

    • Search Google Scholar
    • Export Citation
  • 17.

    Neuhaus SJ, Watson DI, Ellis T, et al. The effect of immune enhancement and suppression on the development of laparoscopic port site metastases. Surg Endosc 2000;14:439443.

    • Search Google Scholar
    • Export Citation
  • 18.

    Burns JM, Matthews BD, Pollinger HS, et al. Effect of carbon dioxide pneumoperitoneum and wound closure technique on port site tumor implantation in a rat model. Surg Endosc 2005;19:441447.

    • Search Google Scholar
    • Export Citation
  • 19.

    Mathew G, Watson DI, Rofe AM, et al. Adverse impact of pneumoperitoneum on intraperitoneal implantation and growth of tumour cell suspension in an experimental model. Aust N Z J Surg 1997;67:289292.

    • Search Google Scholar
    • Export Citation
  • 20.

    Neuhaus SJ, Watson DI, Ellis T, et al. Influence of gases on intraperitoneal immunity during laparoscopy in tumor-bearing rats. World J Surg 2000;24:12271231.

    • Search Google Scholar
    • Export Citation
  • 21.

    Wildbrett P, Oh A, Naundorf D, et al. Impact of laparoscopic gases on peritoneal microenvironment and essential parameters of cell function. Surg Endosc 2003;17:7882.

    • Search Google Scholar
    • Export Citation
  • 22.

    Volz J, Koster S, Spacek Z, et al. Characteristic alterations of the peritoneum after carbon dioxide pneumoperitoneum. Surg Endosc 1999;13:611614.

    • Search Google Scholar
    • Export Citation
  • 23.

    Wong YT, Shah PC, Birkett DH, et al. Carbon dioxide pneumoperitoneum causes severe peritoneal acidosis, unaltered by heating, humidification, or bicarbonate in a porcine model. Surg Endosc 2004;18:14981503.

    • Search Google Scholar
    • Export Citation
  • 24.

    Monnet E, Twedt DC. Laparoscopy. Vet Clin North Am Small Anim Pract 2003;33:11471163.

  • 25.

    Neuhaus SJ, Watson DI, Ellis T, et al. Metabolic and immunologic consequences of laparoscopy with helium or carbon dioxide insufflation: a randomized clinical study. Aust N Z J Surg 2001;71:447452.

    • Search Google Scholar
    • Export Citation
  • 26.

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Contributor Notes

Supported by a grant from Tyco Healthcare.

Address correspondence to Dr. Monnet.