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Advances in Anatomic Pathology:
doi: 10.1097/PAP.0b013e3181aab793
AMR Series

Fatal Systemic Venous Air Embolism During Endoscopic Retrograde Cholangiopancreatography

Bisceglia, Michele MD*; Simeone, Anna MD; Forlano, Rosario MD; Andriulli, Angelo MD§; Pilotto, Alberto MD

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Department of *Pathology

Department of Radiology

Division of Digestive Endoscopy

§Division of Gastroenterology

Division of Geriatrics, Department of Medical Sciences, IRCCS-“Casa Sollievo della Sofferenza” Hospital, Viale Cappuccini, San Giovanni Rotondo (FG), Italy

Reprints: Michele Bisceglia, MD, Department of Pathology, IRCCS-“Casa Sollievo della Sofferenza” Hospital, Viale Cappuccini, San Giovanni Rotondo (FG) I-71013, Italy (e-mail:; figures can be viewed online in color at

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Hepatic portal venous air embolism is the rarest complication of gastrointestinal endoscopy, resulting from penetration of gas into the portal veins, and may occur during endoscopic retrograde cholangiopancreatography and endoscopic biliary sphincterotomy. The likely mechanism is intramural dissection of insufflated air into the portal venous system through duodenal vein radicles transected during the procedure. Hepatic portal air embolism may be fatal. Cerebral air embolism may also occur. So far 13 cases of air embolism after endoscopic retrograde cholangiopancreatography have been reported, with 4 cases of systemic spread that proved fatal. Death was due to pulmonary air embolism in 2 cases, and cerebral air embolism in another 2. We report on an additional such fatal case, concerning a 78-year-old male patient, who several years previously had undergone surgical gastroduodenal resection with cholecystectomy and papillotomy, and was admitted for recurrent ascending cholangitis secondary to bile duct stones. During the third endoscopic cholangioscopic procedure for removal of bile duct stones, sudden cardiopulmonary arrest occurred. Death was due to massive pulmonary air embolism. Cerebral air embolism was also found. Autopsy was performed. A spontaneous duodenobiliary fistula was found. On the basis of bench radiologic investigation (retrograde suprahepatic venography and anterograde portography), it was demonstrated that the air insufflated during duodenal endoscopy, which entered through the spontaneous duodeno-biliary fistula, penetrated into intrahepatic vein radicles injured secondarily to prolonged impaction of biliary sand and stones and infection, resulting in portal and hepatic venous gas and systemic air embolism.

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Diagnosis: Fatal systemic venous air embolism during endoscopic retrograde cholangiopancreatography (ERCP).

Referral Sources: AMR seminar n. 54-case 5 (slides labeled Au-7-03-A and Au-7-03-B), contributed by M. Bisceglia, MD, San Giovanni Rotondo, Italy.

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A 78-year-old male, who several years previously had undergone surgical gastroduodenal resection for duodenal ulcer associated with cholecystectomy and papillotomy, was admitted for recurrent ascending cholangitis secondary to bile duct stones. During hospitalization and while undergoing 2 ERCP procedures for the removal of bile duct stones, he was also diagnosed with chronic lymphocytic leukemia. After 3 months, he underwent a 3rd operative ERCP for recurrent bile duct stones: during this ultimate endoscopic procedure a spontaneous biliary-duodenal fistula was seen and a sudden cardiopulmonary arrest occurred. Imaging studies (computed tomography scan –performed in emergency) demonstrated abundant air in the pulmonary artery, right heart (with air-fluid level), and tributary veins of both superior and inferior vena cava, and in a few intraparenchymal suprahepatic vein radicles of the liver and several biliary ducts (the latter also containing contrast medium) (Figs. 1A–C). Air was seen even in the cerebrocortical veins of the right hemisphere and in the ipsilateral smaller veins of the inner capsule and caudate nucleus, and in the superior ophthalmic veins bilaterally (Figs. 2A, B). Autopsy was performed.

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1. Right heart and pulmonary artery air embolism were confirmed according to appropriate techniques performed in the autopsy room.

2. At cardiac examination no open foramen ovale or other cardiac shunt was seen.

3. The spontaneous bilio-digestive fistula (through which a large amount of gas likely entered the intrahepatic biliary tree) was found while opening the descending portion of the duodenum lengthwise (Fig. 3).

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4. Veno-biliary fistulas were demonstrated according to the following technique: the liver was taken out en-bloc and investigated with retrograde cholangiography (Fig. 4) as well as anterograde portography and retrograde suprahepatic venography via 3 suprahepatic veins (Fig. 5). Bench radiographs, performed in the radiologic operating room, revealed liver intraparenchymal extravasation of the contrast medium (Fig. 4) and reflux-extravasation of the same into the main biliary tree (Fig. 5), where some tufts of cotton wool had been positioned, and which were then radiographed separately (Figs. 6A, B). The contrast medium absorbed by the cotton tufts provided evidence for the presence of small veno-biliary fistulas at both the portal and systemic radicle level.

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5. In the dissection room, on sectioning, the liver cut surface seemed to be punctuated by many parenchymal micro-abscesses containing impacted biliary sand and minute stones (Fig. 7).

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Histologically air bubbles were easily seen in the inspissated bile and in the abscesses of the inflammed portal tracts (Figs. 8A–C, 9A–D). Air bubbles were also present in some blood clots incidentally included in the histologic samples. Some small veins found histologically in the perihepatic soft tissue also showed air embolism (Figs. 10A–D).

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Fatal systemic venous air embolism during endoscopic retrograde cholangiopacreatography.

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Acute, short-term and late complications after gastrointestinal endoscopy are well documented and of diverse types and of varying severity,1 including those related to ERCP and endoscopic biliary sphincterotomy.2–5 Hepatic portal venous air embolism is the rarest complication of gastrointestinal endoscopy, resulting from penetration of gas into the portal veins. Risk factors associated with air embolism in this setting include situations where the mucosa is damaged or where high pressures are generated in the gastrointestinal tract.

Hepatic portal air embolism is a complication that could be seen in the context of various pathologies, including acute mesenteric ischemia,6,7 chronic inflammatory gastrointestinal diseases,8–10 gastrointestinal, abdomino-pelvic, and liver infections,6,9–14 acute gastric dilatation,15 caustic ingestion,16 superior mesenteric artery syndrome with duodenal dilatation,17 ileus,18 blunt abdominal trauma,19,20 pneumatosis cystoides intestinalis, with and without association with trauma,6,21–23 duodeno-caval fistulas,24 and invasive diagnostic procedures, such as double contrast enema (performed in ulcerative colitis or soon after a rectal or colonic biopsy),8 endoscopic sphincterotomy, and ERCP.25 Endoscopic papillotomy and ERCP are almost always performed at the same operative time, the latter as a preliminary guide and/or closing procedure to the former.

The likely mechanism, by which endoscopic sphincterotomy and ERCP may cause air embolism, is the intramural dissection of insufflated air into the portal venous system via venous duodenal radicles, which are inadvertently injured or transected during the procedure. Hepatic portal air embolism is an ominous sign and may be fatal,15,26,27 but may also be reversible or cured by surgery depending on the underlying causes. Cerebral air embolism may also occur during upper gastrointestinal endoscopy,24,28–33 and during or after other invasive endoscopic procedures, mainly bronchoscopy.34–36 Cerebral air embolism may be reversible and the hyperbaric oxygen therapy should always being considered, depending on the severity of the gas embolism and neurologic injury. So far 13 cases of air embolism after ERCP have been reported.25,37–48 Fatal air embolism after liver or biliary procedures or trauma have been recently reviewed by Siddiqui et al.25 The first case of fatal air embolism due to endoscopic sphincterotomy was described in 1988,37 and the first fatal case of systemic air embolism due to ERCP was reported in 1997,42 with a total of 4 systemic fatal cases so far reported.25,42,45,47 Death was due to right ventricle and pulmonary air embolism42 and pulmonary mixed air and bile embolism,25 in one case each, whereas cerebral air embolism was responsible for death in 2 cases.45,47 In our case death was due to massive pulmonary embolism, related to the considerable volume of air found at that level as per clinical manifestations and imaging documentation. However, cerebral air embolism was also significant, and the mechanism by which this occurred is not clear. As cardiac examination did not show any anatomic basis for right to left shunt (paradoxical air embolism), other mechanisms have to be advocated. In these circumstances intrapulmonary shunts and a transcapillary route have been proposed24,49,50 with the latter being active when large air emboli exceed the absorptive capacity of the lung capillary bed. Another possible mechanism for air entering the cerebral veins might have been a retrograde flow into cerebral veins via the superior vena cava.

In conclusion, the air was thought to have entered the venous system via intrahepatic radicles of both the suprahepatic and portal veins, which might have undergone perforation due to chronic ischemic damage of the involved ducts, secondary to prolonged biliary sand/stones impaction and infection. The insufflation which is given during perduodenal endoscopy created the gradient pressure that made air penetrate through the spontaneous bilio-duodenal fistula into the portal and suprahepatic vein radicles, resulting in portal and hepatic venous gas and air embolism. The spontaneous bilio-duodenal fistula likely derived from decubitus pressure of a bile duct stone, which was either previously removed during one of the former ERCPs or passed through into the bowel.

This case has to be added as the most likely dramatic cases of this series of unfortunate events, occasionally fatal, possibly occurring during endoscopic procedures.

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* Very impressive.

* Fatal systemic air embolism after endoscopic retrograde cholangiopancreatography (ERCP) for removal of bile duct stones, associated with ascending cholangitis, cirrhosis of the liver, and chronic lymphatic leukemia. I was not aware of this rare complication of ERCP. Thanks for the contribution.

* Congratulations once more for the discussion in this illustrative case.

* In this case, the slide is less complicated than the story. Asides from the air bubble, the liver looks totally wrecked. I wonder if these complications have any connection with the previous surgical alterations of normal anatomy.

* A nice reminder that seemingly routine cases can go awry! Beautiful images.

* Autopsy material in AMR. That's new in itself.

* Agree with diagnosis. Unusual example where we can actually appreciate air emboli.

* Suppurative ascending cholangiohepatitis. I last saw this as a resident in darkest Africa!

* Agree. As usual, a great presentation.

* Very well documented teaching case, especially for those of us who have to deal with forensic questions.

* I thought it was an infection by gas producing anaerobic bacteria.

* Thanks for very an interesting and educative case. Something like interstitial emphysema in thorax? Air bubbles secondary to gas-forming bacteria? These might be additional possible mechanisms for finding.

* Instructive case.

* A valuable and instructive case. Nothing to add to the peculiar aspect of your case. Just to comment once again that reiterated ERCP is, by itself, a risk factor especially in a patient with ancient gastro-duodenal resection. Years ago I was involved in a malpractice claim where the patient died of postoperative hemorrhage after the 4th ERCP (within a lapse of 40 d). The endoscopist was initially accused of excess of interventionism as long as indication to a repeated procedures was not justified by the clinical evidence of jaundice of undetermined origin, but at the end of the story he was found not guilty.

* As always, an astonishing case.

* Striking appearance!

* Interesting case, thanks.

* The definitive diagnosis that endures this case is the air presence in the heart in the radiology and in the autopsy. Very demonstrative the histologic images of the liver. It is a very rare complication of air embolism.

* Thank you very much for the wonderful case, detailed information and images.

* Great presentation!

* Highly educational case.

* What's for a dramatic complication!

* Nice case.

* Nice autopsy case showing not only the air bubbles related to the embolism, but the prominent microabscesses in the liver, which explain the relevance of the ERCP performed.

* Good case and scholarly discussion. Too bad we cannot confirm the diagnosis by performing an immunohistochemical stain for air!

* Congratulations on solving this mysterious case. I was not aware of this unfortunate complication of ERCP. At our hospital, I'm sure this autopsy would have been sent to the medical examiner's office because of the medicolegal ramifications.

* A typically meticulously studied case. Thanks for the education.

* Iatrogenic air embolism! Wild case. A reminder that every undertaking has a particle of risk!

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portal air embolism; cerebral air embolism; cholangiopancreatography; endoscopy; sphincterotomy; hepatic portal venous gas

© 2009 Lippincott Williams & Wilkins, Inc.


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