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Dr. Leonardo Lidid A y cols. Revista Chilena de Radiología. Vol. 17 Nº 3, 2011; 120-125. Air in periportal space: Beyond the classic triad

Drs. Leonardo Lidid A(1), Sebastián Yévenes A(2), Fabiola Vargas P(2).

1. Assistant Professor of Radiology. West Campus, School of Medicine, University of Chile. San Juan Dios Hospital. Dipreca Hospital Staff.Santiago, Chile. 2. Radiology Resident. West Campus, School of Medicine, University of Chile. San Juan de Dios Hospital.Santiago, Chile.

Abstract: Intrahepatic gas, in particular when located in the bile duct and in the portal vein, has distinctive morphological patterns especially evident on CT studies. This gas, however, may be found not only in these places, but also in the periportal space, a little known extension of the subperitoneal space; it may exhibit intra- hepatic distribution patterns similar to those already described, although with completely different pathological and diagnostic implications. For these reasons we decided to characterize this sign and its CT findings, along with its main differential diagnosis. Keywords: Bile ducts, Cystoides intestinalis, Intestinal perforation, Pneumatosis, Pneumoperitoneum, Portal system, Retroperitoneal space.

Resumen: El gas intrahepático, en particular el ubicado en relación con la vía biliar y la porta, tiene patrones morfológicos característicos especialmente evidentes en los estudios por tomografía computada. El aire,sin embargo, no solamente puede encontrarse en estos lugares, sino que también puede ubicarse en el espacio periportal; una extensión poco conocida del espacio subperitoneal, con patrones de distribución intrahepáticos similares a los ya descritos, pero con implicancias patológicas y diagnósticas completamente diferentes. Por estas razones se decide caracterizar este signo y sus hallazgos en TAC, así como sus principales diagnósticos diferenciales. Palabras clave: Cystoides intestinalis, Ductos Biliares, Espacio Retroperitoneal, Perforación intestinal, Pneumatosis, Pneumoperitoneo, Sistema portal.

Lidid L et al. Aire en el espacio periportal: más allá de la clásica tríada. Rev Chil Radiol 2011; 17 (3): 120-125. Correspondence to: Dr. Leonardo Lidid A. Mailing address: School of Medicine. West Campus. Universidad de Chile. Mail Box 33 052, 33. Santiago [email protected] Manuscript received June 3, 2011, Accepted for publication June 23, 2011.

Introduction of air at this level, its main differential diagnoses, and Gas in the human body may exhibit many distribu- its morphological appearance on axial CT studies. tions, some normal, and some pathological. Concerning the latter, the intrahepatic gas, mainly the one located Periportal space either in the bile duct or in the portal vein, presents The Glisson capsule covers the surface a typical distribution pattern, particularly evident on as an extension of the , except for the CT studies. However, it may also have a very similar bare area. Glisson sheath corresponds to the por- distribution and yet not being directly linked to what is tion of the capsule surrounding the intrahepatic commonly referred to as portal triad. Not only this gas portion of the hepatic portal system (Figure 1A). but also other pathological processes may affect the The portal triad, nerves, and lymphatics (Figure 1b) periportal space, which implies an important range of follow this path of connective tissue through the liver, differential diagnoses, usually ignored when assessing becoming an extension of the subperitoneal space a CT study. In particular, lack of knowledge of this area (subserosal) that comes from the gastrohepatic and appears to have greater importance when working in hepatoduodenal (Figure 2a-b)(1-3). emergency care systems, especially in patients with At hepatic level, the Glisson sheath also continues acute abdominal pathology. These reasons have led to cephalic portion with the subperitoneal space of us to fully describe this space, implications of presence ligamentum teres and falciform (Figure 1a).

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1a 1b

Figure 1. a) Glisson capsule and Glisson sheath. The diagram depicts the continuity of the Glisson sheath, which extends sorrouding the portal vein and its extension through the ligamentum teres and the (see Figure 3). b) Periportal space. The diagram illustrates the portal vein (blue) and the structures of the periportal region which include the hepatic artery (red), bile duct (green), lymphatics (white) and nerves (yellow). Interstitial connective tissue is not represented, but it corresponds to the space between these structures.

2a 2b

Figure 2. a) Anatomical relationship between the portal triad, gastric antrum and duodenal bulb. The gastric antrum and the duodenal bulb are attached to the lesser omentum. b) The liver and the various gastrointestinal tract segments are interconnected by ligaments and . Between the liver and the stomach, gastrohepatic ligaments and the are found. Subperitoneal space is the basis for the potential interconnection between retroperitoneum and . This complex interconnecting space is mainly composed of fatty tissue that contains nerve structures, vessels, and lymphatic tissue surrounded by serous layers which constitute the ligaments and mesenteries associated with the major abdominal organs and viscera. Therefore, it represents an important pathway for disease spread within the peritoneal cavity. The thick arrow in 2a) depicts the possible routes of air spread among the lesser omentum folds, dissecting the periportal space.

Thus, the anatomical continuity of subperito- be observed in periportal location as well as in the liver neal space allows for disease dissemination, fissure (by extension)surrounding the round ligament both among intraperitoneal structures and bet- (Figure 4), and continuing through this pathway even ween extra- and intraperitoneal regions(1,4,5). to its umbilical insertion(1,3,6). Among the pathological phenomena that may use The gas, in this case, is located in the interstitial the periportal route of spread, fluid (edema), blood, tissue that surrounds the portal vein, showing intra inflammatory processes (pancreatic exudates), tu- and extrahepatic distribution (Figure 5). However, both mor infiltrations (Figure 3), and air are included(1-3). the bile duct and the portal vein by themselves may, The latter is often associated, but not limited, to per- under certain conditions, contain air and mimick the forated viscus, mainly of the upper gastrointestinal distribution of above-described findings, especially segment (especially if recent); intrahepatic gas may when there is little air.

121 Dr. Leonardo Lidid A y cols. Revista Chilena de Radiología. Vol. 17 Nº 3, 2011; 120-125.

3a 3b 3c

Figure 3. Patient with peritoneal carcinomatosis of unknown primary site with invasion of periportal space and ligamentum teres. More progressively cephalic slices. b) There is a carcinomatous mass compromising the interior of the lesser sac (arrowheads), ventral to the pancreas (wide arrows), and in c) it invades the hepatic hilum, involving the periportal space (black arrows); it communicates through this with the ligamentum teres (white arrows), which is better seen in b). Liver metastases (*).

4a 4b 4c

4d

Figure 4. Abdominal CT images of a patient aged 73, admitted with epigastric pain and vomiting of two weeks’ duration, secondary to perforated antral ulcer. a-b) Axial and sagittal reconstruction of perforated ulcer (white arrow), which determines communication of gastric lumen (*) to an extraluminal air collection (a) visualized regionally due to omentum with inflammatory phlegmon-like mass(e). A fluid collection (c) in the subserosal space of the lesser omentum (greater curvature) secondary to the above- 4e described perforation is also seen. c-d) Axial reconstructions showing subperitoneal extension of the gas, seen both in the round ligament (white arrowhead) and in thickened periportal interstitial space [periportal edema] (black arrowheads). Initially, periportal free air was viewed as biliary air; however, the intraoperative cholangiogram (not shown) ruled it out. e) Detail of the left hepatic lobe showing a branch of the left portal vein (P), flanked by two hypodensities; the edematized periportal interstitium, partially dissected by air, can be observed(arrowhead).

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5a 5b

5c

Figure 5. Male patient aged 48 with mesenteric ischemia, portal venous air, and subsequent perforated viscus, with subperitoneal air, and severe secondary pneumoperitoneu m. a-b) Axial CT sections showing gas extension through subperitoneal via, adjacent to the pancreas, to the splenic vein (white arrowheads) and through the (double barrel arrow). There is also cephalad spread of air through the hepatoduodenal ligament, adjacent to the common hepatic artery (black arrow head) and its own artery (thick arrow). There is also intraportal gas (arrow) secondary to ischemia. c) Coronal reconstruction that clearly illustrates the extension of gas via hepatoduodenal ligament (thick arrow) (compare with Figure 2a). Gas failed to dissect the intrahepatic fissure; portal air is observed here(arrows). There is also omental and retroperitoneal gas (arrowheads). Pancreatic head (P). Free fluid and pneumoperitoneum (*). (D). Stomach (E). Lesser sac (T).

6a

Portal venous gas Portomesenteric venous gas and its associated finding, i.e., intestinal pneumatosis, represent signs traditionally associated with a poor prognosis since they generally indicate an acute intestinal injury, usually either ischemic or infectious. Nevertheless, anything altering the intestinal wall integrity and causing disrup- tion of the mucosal surface may cause these findings, which include pathological dilatation of bowel loops, 6b intestinal ulcers, trauma, inflammatory bowel disease, and surgical procedures, among others. Likewise, there are a number of benign diagnoses that may be associated with this signology, so it is higly relevant to consider the clinical context of each individual patient(7,8). On CT scans, images of air-filled tubular structu- res may be observed; they ramify from the center toward the periphery of the liver, even to reach the capsule of this organ (Figure 6 ab) (8,9,10). Then, depending on its volume, the air tends to have an antigravitational distribution, predominantly in the left liver lobe. Associated findings such as pneumatosis intestinalis may also be observed (Figure 6 c-d)(7).

123 Dr. Leonardo Lidid A y cols. Revista Chilena de Radiología. Vol. 17 Nº 3, 2011; 120-125.

6c 6d

Figure 6. Portal venous air. Same patient as in Figure 5. a) Scout view depicting pneumoperitoneum and portal venous air. It is hard to define if gas is actually located in the portal vein (white arrows). Usually, the radiographic image appears to be relatively nonspecific for this diagnosis, since it is often confused with aerobilia. Gas location is easier to be determined on axial slices. b). Axial computed tomography image showing the portal vein (P) with air (white arrows) reaching the capsule of the left hepatic lobe, pneumoperitoneum, and free fluid (*). c) Axial CT slices at a still more caudal level, showing pathological loop dilatation with parietal thickening, and pneumatosis. Note how intramural gas (arrows) is separated from the bowel lumen (L), which becomes more evident in d) due to its antigravitational position (arrow). Free subphrenic and interloop fluid and interloops are also observed.

Gas in the biliary tract (aerobilia) It refers to the accumulation of air in the biliary tree secondary to multiple causes, being the most frequent ones surgical biliary-enteric anastomosis, spontaneous biliary-enteric fistulas, and incompe- tence of the sphincter of Oddi (commonly iatroge- 7b nic, secondary to post ERCP sphincterotomy, and rarely due to non-iatrogenic causes, e.g., secondary to recent passage of stones, among others). Less common causes include infections (cholangitis), and bronchopleural fistula(9). On CT studies, gas has a typical distribution on the Scout view (Figure 7 a) that correlates perfectly with its morphology in the axial slices, where it is dis- played as branches with air density that tend to have a more central location, converging in the (due to centripetal flow of bile) (Figure 7 b-c), preferably occupying the left hepatic lobe, as described concerning air in the portal vein. Due to bile flow distribution, air in the periphery rarely extends to within 2 cm of the liver capsule (Figure 7d)(9,11,12).

7a 7c

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7d i.e., portal and biliary air, since its etiology and clinical outcome are completely different.

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