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Carbon dioxide embolism during laparoscopic cholecystectomy due to a patent paraumbilical vein
Journal of Pediatric Surgery (2007) 42, 570 – 572
www.elsevier.com/locate/jpedsurg
Carbon dioxide embolism during laparoscopic cholecystectomy due to a patent paraumbilical vein Peter Matteia,*, Donald C. Tylerb a
Pediatric General, Thoracic and Fetal Surgery, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA Department of Anesthesiology and Critical Care Medicine, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA b
Index words: Laparoscopy; Complications; Carbon dioxide; Gas embolism; End-tidal CO2
Abstract Carbon dioxide embolism is a rare but potentially fatal complication of laparoscopic surgery. The most common cause is inadvertent injection of carbon dioxide into a large vein or solid organ during initial peritoneal insufflation. We describe a case of carbon dioxide embolism in a 13-year-old boy during an elective laparoscopic cholecystectomy, caused by injection of carbon dioxide into a large paraumbilical vein. The clinical manifestations of carbon dioxide embolism were hypotension, bradycardia, and an abrupt drop in end-tidal CO2. He subsequently did well and had no sequelae. Carbon dioxide embolism is a recognized complication of laparoscopic surgery, although the risk to the patient may be minimized by the surgical team’s awareness of the problem, continuous intraoperative monitoring of end-tidal CO2, and using an open technique for initial access to the peritoneum. D 2007 Elsevier Inc. All rights reserved.
Carbon dioxide embolism can occur during laparoscopic procedures, most commonly from inadvertent injection of carbon dioxide into a large vein or intraabdominal organ during initial insufflation. Although often without adverse sequelae, such emboli are potentially fatal. We describe an unusual case of carbon dioxide embolism thought to be caused by injection of the gas into a patent paraumbilical vein during laparoscopic cholecystectomy in a 13-year-old boy.
1. Case report A 13-year-old boy presented with a 3-week history of intermittent right upper quadrant abdominal pain. The pain
* Corresponding author. Department of Surgery, University of Pennsylvania School of Medicine, PA, USA. Tel.: +1 215 590 4981; fax: +1 215 386 4036. E-mail address: [email protected] (P. Mattei). 0022-3468/$ – see front matter D 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.jpedsurg.2006.10.051
was exacerbated by meals and accompanied by nausea. Physical examination findings were normal, with no stigmata of liver disease or portal hypertension. Liver function studies were within normal limits. Ultrasound examination revealed several small gallstones and a 5-mm common bile duct. His past medical history was significant for acute lymphoblastic leukemia at age 3 and a relapse at age 9; however, he was in remission and doing well for 4 years. While receiving methotrexate and etoposide for relapsed acute lymphoblastic leukemia, he developed veno-occlusive disease of the liver, with acute hepatic dysfunction, ascites, and splenomegaly. This eventually resolved without apparent sequelae, and subsequent Doppler ultrasound examination revealed normalization of hepatic blood flow, complete resolution of ascites, and a normal spleen. The patient was premedicated with oral midazolam, and, after induction with sevoflurane, he was given vecuronium
Carbon dioxide embolism during laparoscopic cholecystectomy due to a patent paraumbilical vein and intubated. An orogastric tube was placed, and before incision he received clindamycin and gentamicin. Anesthesia was maintained with desflurane and intravenous morphine. Abdominal insufflation was performed by using a closed technique through a 10-mm infraumbilical incision. The fascia was controlled with Kocher clamps, a Veress needle was inserted at a cephalad angle, and, after a saline drop test was successfully performed, insufflation with carbon dioxide was started at low flow. Within seconds, the insufflation pressure was noted to be higher than expected and the Veress needle was immediately removed. The patient abruptly developed hypotension and bradycardia, and the end-tidal CO2 dropped from 31 to 15 mm Hg (Fig. 1). He was not wheezing, and no rash was noted. He was quickly placed in the Trendelenberg position and given ephedrine and a bolus of saline. Over the course of about 10 minutes, the blood pressure and heart rate normalized and the end-tidal CO2 returned to 26 to 30. The Veress needle was reinserted at a less cephalad angle and the abdomen was insufflated without difficulty. The patient remained stable throughout the remainder of the operation. Although the liver was normal in appearance, the gallbladder bed was more vascular than expected and blood loss was approximately 100 mL. A trickle of blood was noted from the umbilical port site throughout the procedure, and upon removal of the trocar at the end of the operation, brisk bleeding was noted from the incision. The source of bleeding was a large vein in the falciform ligament that had the appearance of a patent umbilical vein. It was easily controlled and ligated. The patient recovered uneventfully and was discharged the next day. On routine follow up 4 weeks after surgery he was asymptomatic and doing well.
571
2. Discussion Clinically significant gas embolism is thought to occur in less than 0.6% of laparoscopic operations [1]. Using transesophageal echocardiography to detect gas bubbles in the right side of the heart, Derouin et al [2] found evidence of subclinical gas embolism during 11 of 16 laparoscopic cholecystectomies (5 during insufflation, 6 during gallbladder dissection), suggesting that the true incidence of occult CO2 embolism may actually be higher. Although usually well tolerated [3], gas embolism can be fatal in up to 28% of reported cases in adults [4-7]. The incidence in children is not known. A large quantity of gas in the right ventricle can cause circulatory collapse caused by disruption of pump function or bgas lockQ [8]. Carbon dioxide is much less toxic than air because of its high solubility in the blood [9]; however, a large bolus can result in identical pathophysiology. The clinical manifestations of gas embolism include hypotension and bradycardia. A bmachineryQ murmur may be identified and is pathognomic of the diagnosis. An intraoperative CO2 embolism typically causes a sudden drop in end-tidal CO2, as occurred in our patient. The initial treatment of a suspected CO2 embolism is immediate cessation of insufflation. It is recommended that the patient be positioned with the head down and the right side up (Durant’s position) [9,10] to allow the gas to accumulate in the apex and away from the outlet of the right ventricle. Cardiopulmonary resuscitation may be indicated for persistent hypotension or arrhythmia. Some have recommended the insertion of a long central venous catheter to aspirate the gas directly from the right ventricle [11]. A bolus of carbon dioxide can enter the circulation by direct injection of the gas into a vessel or parenchymal
Fig. 1 Intraoperative end-tidal CO2 measurements: End-tidal CO2 was measured continuously and recorded at intervals by an automated anesthesia-recording system (CompuRecord, Koninklijke Philips Electronics, Amsterdam, The Netherlands). The tics at the bottom of the graph represent time of procedure start and time of incision. Within minutes of inserting the Veress needle and beginning insufflation with carbon dioxide, the patient became hypotensive and the end-tidal CO2 dropped precipitously. Insufflation was stopped immediately; within several minutes, the blood pressure returned to normal and the end-tidal CO2 returned to baseline.
572 organ or by entry of gas under pressure through an injured vein [7,12]. The incidence of direct injection might be reduced by using an open (Hasson) technique [5], but there are few data to confirm this [13]. When the Veress needle is used, it is recommended that the initial insufflation be performed using low flow to prevent a large bolus [1]. The entry of gas through an injured vein has also occurred during hepatic resection and living related-donor nephrectomy [7]. The pneumoperitoneum should be maintained at the lowest possible pressure and the surgeon should be prepared to control large venous bleeding rapidly. Our patient is thought to have had a carbon dioxide embolism caused by injection of the gas into a large anomalous vein that was located in the free edge of the falciform ligament. The umbilical vein delivers blood from the placenta into the central circulation via the intrahepatic ductus venosus, and closes shortly after birth, becoming the ligamentum teres hepatis. Patients with portal hypertension can develop a portosystemic shunt in the form of a bpatent umbilical veinQ [14,15]. It has been suggested, however, that the umbilical vein never recanalizes and that it is actually one of the paraumbilical veins that becomes enlarged in this setting [16]. These are venous tributaries that run parallel to the ligamentum teres hepatis and stay patent into adulthood [17]. Our patient had a history of veno-occlusive disease while receiving chemotherapy [18,19], and although he currently has no clinical signs of portal hypertension, we believe this may account for the persistence of an enlarged paraumbilical vein. Persistent mild portal venous congestion may also account for the relative difficulty of the operation. Injury of the paraumbilical veins during laparoscopy has been described [20,21]; however, this is the first report of a gas embolism owing to a patent paraumbilical vein. Presumably because of vagal stimulation by increased intraabdominal pressure, bradycardia and hypotension has been noted to occur in up to 4.7% of laparoscopic cholecystectomies [22]. This might explain what occurred in our patient; however, the extremely rapid onset, the severe drop in the end-tidal CO2, and the presence of a large vein at the site of Veress needle insertion argue in favor of gas embolism as the cause. In summary, carbon dioxide embolism is a rare but potentially serious complication of laparoscopy. Inadvertent injection of carbon dioxide into a vein during peritoneal insufflation is the most common cause. We describe an unusual case of carbon dioxide embolism during laparoscopic cholecystectomy in a 13-year-old boy who had a large paraumbilical vein. Intraoperative gas embolism presents with hypotension and a sharp drop in end-tidal CO2. Treatment includes immediate cessation of carbon dioxide insufflation, placing the patient in a steep Trendelenberg (head-down) position, and resuscitative measures as necessary. The incidence of gas embolism may be lower when peritoneal insufflation is performed using an open technique rather than with a Veress needle.
P. Mattei, D.C. Tyler
References [1] Neudecker J, Sauerland S, Neugebauer E, et al. The European Association for Endoscopic Surgery clinical practice guideline on the pneumoperitoneum for laparoscopic surgery. Surg Endosc 2002;16(7): 1121 - 43. [2] Derouin M, Couture P, Boudreault D, et al. Detection of gas embolism by transesophageal echocardiography during laparoscopic cholecystectomy. Anesth Analg 1996;82(1):119 - 24. [3] Veyckemans F. Celioscopic surgery in infants and children: the anesthesiologist’s point of view. Paediatr Anaesth 2004;14(5): 424 - 32. [4] Cottin V, Delafosse B, Viale JP. Gas embolism during laparoscopy: a report of seven cases in patients with previous abdominal surgical history. Surg Endosc 1996;10(2):166 - 9. [5] Magrina JF. Complications of laparoscopic surgery. Clin Obstet Gynecol 2002;45(2):469 - 80. [6] Lantz PE, Smith JD. Fatal carbon dioxide embolism complicating attempted laparoscopic cholecystectomy—case report and literature review. [see comment]J Forensic Sci 1994;39(6):1468 - 80. [7] Boghossian T, Henri M, Dube S, et al. Laparoscopic nephrectomy donor death due to cerebral gas embolism in a specialized transplant center: risk zero does not exist. Transplantation 2005;79(2):258 - 9 [see comment]. [8] Gutt CN, Oniu T, Mehrabi A, et al. Circulatory and respiratory complications of carbon dioxide insufflation. Dig Surg 2004;21(2): 95 - 105. [9] Cobb WS, Fleishman HA, Kercher KW, et al. Gas embolism during laparoscopic cholecystectomy. J Laparoendosc Adv Surg Tech A 2005;15(4):387 - 90. [10] Joshi GP. Complications of laparoscopy. Anesthesiol Clin North America 2001;19(1):89 - 105. [11] Zhang W, Ho KS, Han HJ, et al. Successful resuscitation after carbon dioxide embolism during laparoscopic-assisted abdomino-perineal resection. Singapore Med J 2005;46(7):347 - 8. [12] Councilman-Gonzales LM, Bean-Lijewski JD, McAllister RK. A probable CO2 embolus during laparoscopic cholecystectomy. Can J Anaesth 2003;50(3):313. [13] Bonjer HJ, Hazebroek EJ, Kazemier G, et al. Open versus closed establishment of pneumoperitoneum in laparoscopic surgery. Br J Surg 1997;84(5):599 - 602. [14] Martin BF, Tudor RG. The umbilical and paraumbilical veins of man. J Anat 1980;130(Pt 2):305 - 22. [15] Merkle EM, Gilkeson RC. Remnants of fetal circulation: appearance on MDCT in adults. AJR Am J Roentgenol 2005;185(2):541 - 9. [16] Lafortune M, Constantin A, Breton G, et al. The recanalized umbilical vein in portal hypertension: a myth. AJR Am J Roentgenol 1985;144(3):549 - 53. [17] Horton KM, Fishman EK. Paraumbilical vein in the cirrhotic patient: imaging with 3D CT angiography. Abdom Imaging 1998;23(4): 404 - 8. [18] Ribaud P, Gluckman E. Hepatic veno-occlusive disease. Pediatr Transplant 1999;3(Suppl 1):41 - 4. [19] Reiss U, Cowan M, McMillan A, et al. Hepatic venoocclusive disease in blood and bone marrow transplantation in children and young adults: incidence, risk factors, and outcome in a cohort of 241 patients. J Pediatr Hematol/Oncol 2002;24(9):746 - 50 [see comment]. [20] Goldstein AM, Gorlick N, Gibbs D, et al. Hemoperitoneum due to spontaneous rupture of the umbilical vein. Am J Gastroenterol 1995; 90(2):315 - 7. [21] Salmi A. Laparoscopic rupture of a patent umbilical vein. Gastrointest Endosc 1986;32(5):374. [22] Reed DNJ, Duff JL. Persistent occurrence of bradycardia during laparoscopic cholecystectomies in low-risk patients. Dig Surg 2000;17(5):513 - 7.
www.elsevier.com/locate/jpedsurg
Carbon dioxide embolism during laparoscopic cholecystectomy due to a patent paraumbilical vein Peter Matteia,*, Donald C. Tylerb a
Pediatric General, Thoracic and Fetal Surgery, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA Department of Anesthesiology and Critical Care Medicine, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA b
Index words: Laparoscopy; Complications; Carbon dioxide; Gas embolism; End-tidal CO2
Abstract Carbon dioxide embolism is a rare but potentially fatal complication of laparoscopic surgery. The most common cause is inadvertent injection of carbon dioxide into a large vein or solid organ during initial peritoneal insufflation. We describe a case of carbon dioxide embolism in a 13-year-old boy during an elective laparoscopic cholecystectomy, caused by injection of carbon dioxide into a large paraumbilical vein. The clinical manifestations of carbon dioxide embolism were hypotension, bradycardia, and an abrupt drop in end-tidal CO2. He subsequently did well and had no sequelae. Carbon dioxide embolism is a recognized complication of laparoscopic surgery, although the risk to the patient may be minimized by the surgical team’s awareness of the problem, continuous intraoperative monitoring of end-tidal CO2, and using an open technique for initial access to the peritoneum. D 2007 Elsevier Inc. All rights reserved.
Carbon dioxide embolism can occur during laparoscopic procedures, most commonly from inadvertent injection of carbon dioxide into a large vein or intraabdominal organ during initial insufflation. Although often without adverse sequelae, such emboli are potentially fatal. We describe an unusual case of carbon dioxide embolism thought to be caused by injection of the gas into a patent paraumbilical vein during laparoscopic cholecystectomy in a 13-year-old boy.
1. Case report A 13-year-old boy presented with a 3-week history of intermittent right upper quadrant abdominal pain. The pain
* Corresponding author. Department of Surgery, University of Pennsylvania School of Medicine, PA, USA. Tel.: +1 215 590 4981; fax: +1 215 386 4036. E-mail address: [email protected] (P. Mattei). 0022-3468/$ – see front matter D 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.jpedsurg.2006.10.051
was exacerbated by meals and accompanied by nausea. Physical examination findings were normal, with no stigmata of liver disease or portal hypertension. Liver function studies were within normal limits. Ultrasound examination revealed several small gallstones and a 5-mm common bile duct. His past medical history was significant for acute lymphoblastic leukemia at age 3 and a relapse at age 9; however, he was in remission and doing well for 4 years. While receiving methotrexate and etoposide for relapsed acute lymphoblastic leukemia, he developed veno-occlusive disease of the liver, with acute hepatic dysfunction, ascites, and splenomegaly. This eventually resolved without apparent sequelae, and subsequent Doppler ultrasound examination revealed normalization of hepatic blood flow, complete resolution of ascites, and a normal spleen. The patient was premedicated with oral midazolam, and, after induction with sevoflurane, he was given vecuronium
Carbon dioxide embolism during laparoscopic cholecystectomy due to a patent paraumbilical vein and intubated. An orogastric tube was placed, and before incision he received clindamycin and gentamicin. Anesthesia was maintained with desflurane and intravenous morphine. Abdominal insufflation was performed by using a closed technique through a 10-mm infraumbilical incision. The fascia was controlled with Kocher clamps, a Veress needle was inserted at a cephalad angle, and, after a saline drop test was successfully performed, insufflation with carbon dioxide was started at low flow. Within seconds, the insufflation pressure was noted to be higher than expected and the Veress needle was immediately removed. The patient abruptly developed hypotension and bradycardia, and the end-tidal CO2 dropped from 31 to 15 mm Hg (Fig. 1). He was not wheezing, and no rash was noted. He was quickly placed in the Trendelenberg position and given ephedrine and a bolus of saline. Over the course of about 10 minutes, the blood pressure and heart rate normalized and the end-tidal CO2 returned to 26 to 30. The Veress needle was reinserted at a less cephalad angle and the abdomen was insufflated without difficulty. The patient remained stable throughout the remainder of the operation. Although the liver was normal in appearance, the gallbladder bed was more vascular than expected and blood loss was approximately 100 mL. A trickle of blood was noted from the umbilical port site throughout the procedure, and upon removal of the trocar at the end of the operation, brisk bleeding was noted from the incision. The source of bleeding was a large vein in the falciform ligament that had the appearance of a patent umbilical vein. It was easily controlled and ligated. The patient recovered uneventfully and was discharged the next day. On routine follow up 4 weeks after surgery he was asymptomatic and doing well.
571
2. Discussion Clinically significant gas embolism is thought to occur in less than 0.6% of laparoscopic operations [1]. Using transesophageal echocardiography to detect gas bubbles in the right side of the heart, Derouin et al [2] found evidence of subclinical gas embolism during 11 of 16 laparoscopic cholecystectomies (5 during insufflation, 6 during gallbladder dissection), suggesting that the true incidence of occult CO2 embolism may actually be higher. Although usually well tolerated [3], gas embolism can be fatal in up to 28% of reported cases in adults [4-7]. The incidence in children is not known. A large quantity of gas in the right ventricle can cause circulatory collapse caused by disruption of pump function or bgas lockQ [8]. Carbon dioxide is much less toxic than air because of its high solubility in the blood [9]; however, a large bolus can result in identical pathophysiology. The clinical manifestations of gas embolism include hypotension and bradycardia. A bmachineryQ murmur may be identified and is pathognomic of the diagnosis. An intraoperative CO2 embolism typically causes a sudden drop in end-tidal CO2, as occurred in our patient. The initial treatment of a suspected CO2 embolism is immediate cessation of insufflation. It is recommended that the patient be positioned with the head down and the right side up (Durant’s position) [9,10] to allow the gas to accumulate in the apex and away from the outlet of the right ventricle. Cardiopulmonary resuscitation may be indicated for persistent hypotension or arrhythmia. Some have recommended the insertion of a long central venous catheter to aspirate the gas directly from the right ventricle [11]. A bolus of carbon dioxide can enter the circulation by direct injection of the gas into a vessel or parenchymal
Fig. 1 Intraoperative end-tidal CO2 measurements: End-tidal CO2 was measured continuously and recorded at intervals by an automated anesthesia-recording system (CompuRecord, Koninklijke Philips Electronics, Amsterdam, The Netherlands). The tics at the bottom of the graph represent time of procedure start and time of incision. Within minutes of inserting the Veress needle and beginning insufflation with carbon dioxide, the patient became hypotensive and the end-tidal CO2 dropped precipitously. Insufflation was stopped immediately; within several minutes, the blood pressure returned to normal and the end-tidal CO2 returned to baseline.
572 organ or by entry of gas under pressure through an injured vein [7,12]. The incidence of direct injection might be reduced by using an open (Hasson) technique [5], but there are few data to confirm this [13]. When the Veress needle is used, it is recommended that the initial insufflation be performed using low flow to prevent a large bolus [1]. The entry of gas through an injured vein has also occurred during hepatic resection and living related-donor nephrectomy [7]. The pneumoperitoneum should be maintained at the lowest possible pressure and the surgeon should be prepared to control large venous bleeding rapidly. Our patient is thought to have had a carbon dioxide embolism caused by injection of the gas into a large anomalous vein that was located in the free edge of the falciform ligament. The umbilical vein delivers blood from the placenta into the central circulation via the intrahepatic ductus venosus, and closes shortly after birth, becoming the ligamentum teres hepatis. Patients with portal hypertension can develop a portosystemic shunt in the form of a bpatent umbilical veinQ [14,15]. It has been suggested, however, that the umbilical vein never recanalizes and that it is actually one of the paraumbilical veins that becomes enlarged in this setting [16]. These are venous tributaries that run parallel to the ligamentum teres hepatis and stay patent into adulthood [17]. Our patient had a history of veno-occlusive disease while receiving chemotherapy [18,19], and although he currently has no clinical signs of portal hypertension, we believe this may account for the persistence of an enlarged paraumbilical vein. Persistent mild portal venous congestion may also account for the relative difficulty of the operation. Injury of the paraumbilical veins during laparoscopy has been described [20,21]; however, this is the first report of a gas embolism owing to a patent paraumbilical vein. Presumably because of vagal stimulation by increased intraabdominal pressure, bradycardia and hypotension has been noted to occur in up to 4.7% of laparoscopic cholecystectomies [22]. This might explain what occurred in our patient; however, the extremely rapid onset, the severe drop in the end-tidal CO2, and the presence of a large vein at the site of Veress needle insertion argue in favor of gas embolism as the cause. In summary, carbon dioxide embolism is a rare but potentially serious complication of laparoscopy. Inadvertent injection of carbon dioxide into a vein during peritoneal insufflation is the most common cause. We describe an unusual case of carbon dioxide embolism during laparoscopic cholecystectomy in a 13-year-old boy who had a large paraumbilical vein. Intraoperative gas embolism presents with hypotension and a sharp drop in end-tidal CO2. Treatment includes immediate cessation of carbon dioxide insufflation, placing the patient in a steep Trendelenberg (head-down) position, and resuscitative measures as necessary. The incidence of gas embolism may be lower when peritoneal insufflation is performed using an open technique rather than with a Veress needle.
P. Mattei, D.C. Tyler
References [1] Neudecker J, Sauerland S, Neugebauer E, et al. The European Association for Endoscopic Surgery clinical practice guideline on the pneumoperitoneum for laparoscopic surgery. Surg Endosc 2002;16(7): 1121 - 43. [2] Derouin M, Couture P, Boudreault D, et al. Detection of gas embolism by transesophageal echocardiography during laparoscopic cholecystectomy. Anesth Analg 1996;82(1):119 - 24. [3] Veyckemans F. Celioscopic surgery in infants and children: the anesthesiologist’s point of view. Paediatr Anaesth 2004;14(5): 424 - 32. [4] Cottin V, Delafosse B, Viale JP. Gas embolism during laparoscopy: a report of seven cases in patients with previous abdominal surgical history. Surg Endosc 1996;10(2):166 - 9. [5] Magrina JF. Complications of laparoscopic surgery. Clin Obstet Gynecol 2002;45(2):469 - 80. [6] Lantz PE, Smith JD. Fatal carbon dioxide embolism complicating attempted laparoscopic cholecystectomy—case report and literature review. [see comment]J Forensic Sci 1994;39(6):1468 - 80. [7] Boghossian T, Henri M, Dube S, et al. Laparoscopic nephrectomy donor death due to cerebral gas embolism in a specialized transplant center: risk zero does not exist. Transplantation 2005;79(2):258 - 9 [see comment]. [8] Gutt CN, Oniu T, Mehrabi A, et al. Circulatory and respiratory complications of carbon dioxide insufflation. Dig Surg 2004;21(2): 95 - 105. [9] Cobb WS, Fleishman HA, Kercher KW, et al. Gas embolism during laparoscopic cholecystectomy. J Laparoendosc Adv Surg Tech A 2005;15(4):387 - 90. [10] Joshi GP. Complications of laparoscopy. Anesthesiol Clin North America 2001;19(1):89 - 105. [11] Zhang W, Ho KS, Han HJ, et al. Successful resuscitation after carbon dioxide embolism during laparoscopic-assisted abdomino-perineal resection. Singapore Med J 2005;46(7):347 - 8. [12] Councilman-Gonzales LM, Bean-Lijewski JD, McAllister RK. A probable CO2 embolus during laparoscopic cholecystectomy. Can J Anaesth 2003;50(3):313. [13] Bonjer HJ, Hazebroek EJ, Kazemier G, et al. Open versus closed establishment of pneumoperitoneum in laparoscopic surgery. Br J Surg 1997;84(5):599 - 602. [14] Martin BF, Tudor RG. The umbilical and paraumbilical veins of man. J Anat 1980;130(Pt 2):305 - 22. [15] Merkle EM, Gilkeson RC. Remnants of fetal circulation: appearance on MDCT in adults. AJR Am J Roentgenol 2005;185(2):541 - 9. [16] Lafortune M, Constantin A, Breton G, et al. The recanalized umbilical vein in portal hypertension: a myth. AJR Am J Roentgenol 1985;144(3):549 - 53. [17] Horton KM, Fishman EK. Paraumbilical vein in the cirrhotic patient: imaging with 3D CT angiography. Abdom Imaging 1998;23(4): 404 - 8. [18] Ribaud P, Gluckman E. Hepatic veno-occlusive disease. Pediatr Transplant 1999;3(Suppl 1):41 - 4. [19] Reiss U, Cowan M, McMillan A, et al. Hepatic venoocclusive disease in blood and bone marrow transplantation in children and young adults: incidence, risk factors, and outcome in a cohort of 241 patients. J Pediatr Hematol/Oncol 2002;24(9):746 - 50 [see comment]. [20] Goldstein AM, Gorlick N, Gibbs D, et al. Hemoperitoneum due to spontaneous rupture of the umbilical vein. Am J Gastroenterol 1995; 90(2):315 - 7. [21] Salmi A. Laparoscopic rupture of a patent umbilical vein. Gastrointest Endosc 1986;32(5):374. [22] Reed DNJ, Duff JL. Persistent occurrence of bradycardia during laparoscopic cholecystectomies in low-risk patients. Dig Surg 2000;17(5):513 - 7.