IMAGING THE HEPATIC LYMPHATICS: EXPERIMENTAL STUDIES …€¦ · IMAGINGTHEHEPATIC LYMPHATICS:EXPERIMENTAL STUDIESINSWINE JamesD. Collins, MD,Anthony C. Disher, MD, Maria L. Shaver,

IMAGING THE HEPATICLYMPHATICS: EXPERIMENTALSTUDIES IN SWINEJames D. Collins, MD, Anthony C. Disher, MD, Maria L. Shaver, MD, and Theodore Q. Miller, MDLos Angeles, California

Magnetic resonance (MR) imaging augmentedwith 3-D MR reconstruction provides an excel-lent display of the soft tissues and surfaceanatomy of the human body. The excellentanatomical detail of MR images makes thisradiographic modality an ideal tool to teachanatomy to all health-care professionals.

Previous studies of the lung and liver inswine revealed that the hepatic lymphaticscommunicated with the visceral pleural lym-phatics via the so-called pulmonary ligament,which appears as a sheet of visceral pleuracontaining lymphatics and small blood vesselsin the swine model. A review of the surgicaloperative reports at the UCLA School of Medi-cine revealed that the hepatic lymphatics arenot connected or even ligated during hepaticresections and transplantations. Therefore, theauthors hypothesized that the unattached lym-phatics may be a cause of postoperativecomplications and that interruption of theseimportant lymphatic pathways may specificallyresult in immediate ascites and right pleuraleffusions. Cannulation of the hepatic lymphat-ics is proposed as a method to reduce postop-erative complications.The purpose of this research is to demon-

strate the visual and radiographic display of

From the Department of Radiological Sciences, UCLA Schoolof Medicine, Los Angeles, California. Presented at the 104thAnnual American Association of Anatomists Meeting, April20-24, 1991, Chicago, Illinois, and the 97th Annual Conventionof the National Medical Association, June 29-Aug 4, 1991,Indianapolis, Indiana. Research performed in the Leo G. RiglerResearch Center for Radiological Sciences. Reprint requestsshould be addressed to Dr James D. Collins, Dept ofRadiological Sciences, UCLA Center for the Health Sciences,Los Angeles, CA 90024-1721.

the hepatic lymphatics in a swine model and toprovide a means to teach anatomical-pathological correlation. (J Nat! Med Assoc.1993;85:185-191.)

Key words * magnetic resonance imaging (MRI).Ethiodol oil * swine liver* transplantation * lymphatics

Traditionally, the radiologist has used plain films,intravascular contrast agents, and radiopharmaceuticalsto image the liver. Hepatic lymphatics have beenaccidentally imaged during percutaneous transhepaticcholangiograms. They appeared on the fluoroscopicscreen as small, linear, slowly emptying structuresparalleling larger veins. These lymphatics seemed tohave no apparent communication or definite anatomicpathways. Because the hepatic lymphatics have notbeen studied extensively, the importance of thesestructures has remained a curiosity to the anatomist,pathologist, and inquisitive radiologist who occasion-ally imaged them.

With the advent of computerized radiographic imag-ing (computerized tomography [CT], ultrasonography,magnetic resonance imaging [MRI], 3-D reconstruc-tion, cine-MR, and SPECT nuclear medicine), there hasbeen a virtual explosion of methods for the radiologistto image the liver in a noninvasive fashion. We haveused MRI to study the lymphatics of the lung and theliver in a swine model.1 2 In these previous reports, weobserved that the hepatic lymphatics communicatedwith the visceral pleural lymphatics via the so-calledpulmonary ligament, which appears as a sheet ofvisceral pleura containing lymphatics and small bloodvessels in the swine model. This observation wasconfirmed by the senior author (JDC) during hisparticipation at many human autopsies. Moreover,dilated lymphatics in liver transplantation and cancer

JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 85, NO. 3 185

HEPATIC LYMPHATICS IN SWINE

Figure 1. The gross specimen of the swine liver demonstrating the four lobes (1, li, lit,IV). Anastomosing lymphatics (arrows) and vascular structures are contiguous with thefascia and inferior surface of the diaphragm (GB=gallbladder and D=diaphragm).Figure 2. The visceral surface demonstrating fat radiating from the lobes of the liver.The lymphatics (arrows) anastomose with hepatic lobules (PH=portahepatis andLN = lymph node). Figure 3. One edge of the liver demonstrating the benzene-likestructures of the hepatic lobules. Lymphatics (arrows) marginate the liver edgeinterdigitating with the hepatic lobules. Figure 4. A retrograde saline injection of acapsular lymphatic. Note the filling of the adjacent collateral lymphatics circumscribingthe hepatic lobules. Marginal lymphatics are dilated (arrows). Figure 5. The salineinjection into a large surface lymphatic (untied) of the gallbladder. Saline hasextravasated around the needle. Note areas of constrictions (lymph valves). Vascularstructures parallel the dilated transparent lymphatics (arrows) (GB= gallbladder andVN = Viamonte needle). Figure 6. Saline has been inected into visceral surfacelymphatics (tied) to demonstrate collateralization (arrows) with the hepatic lobules andlymph nodes (GB=gallbladder). Figure 7. Radiograph demonstrating oily contrastinjected into the capsular lymphatic of Figure 4. Interlobular and marginal lymphatics(arrows) are filled. Extravasation (arrow with crossbar) has occurred at the injection site(GB =gallbladder and PH = portahepatis).

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patients have been demonstrated on CT images of theliver as low-density areas surrounding the intrahepaticbile ducts.3We have cannulated swine lung lymphatics with

small and large needles, injected contrast, and imagedthese lymphatics with plain radiography, CT, and MRI.Therefore, it would seem logical that the hepaticlymphatics could be cannulated, contrast injected, andimaged by similar methods. We were successful in thisendeavor.

This article describes a hepatic lymphatic cannula-tion technique with radiographic images of the contrastinjected swine liver model. We present this research todemonstrate a visual radiographic display of hepaticlymphatic pathways using various radiographic modali-ties and to provide a model that may be used to teachanatomical-pathological correlation to health-care pro-fessionals.

METHODS AND MATERIALSFifteen adult Red Duroc swine (40 kg to 45 kg) were

given preoperative ketamine and lidocaine before beingplaced on the fluoroscopic table. An 8-mm endotracheal

tube was inserted proximal to the division of the tracheaunder fluoroscopic control. The tube was secured byinflating the endotracheal cuff. An Ohio ventilator(Ohio Medical Products, a Division of Airco Inc,Madison, Wisconsin) was used to administer halothanefor general anesthesia.A vertical incision was then made from the level of

the thyroid cartilage to approximately 25 cm below thexyphoid process. Blunt dissection was performed downto the fascial planes of the neck, mediastinum, and theupper abdomen. The major blood vessels of the neck,thorax, and upper abdomen were tied off with 4.0 silkligatures in order to maintain a clear field of vision toharvest the lungs, heart, and liver. The esophagus andthe thoracic duct also were tied off with 4.0 silk. Theinferior visceral pleural reflection from the pulmonaryhila to the diaphragm was preserved along with thediaphragm. This was accomplished to maintain thelymphatic drainage from the abdomen and the dia-phragm. The lungs, heart, and liver were then harvested,and the swine were killed with an intravenous injectionof phenobarbital and exsanguination.

The liver and diaphragms were separated from the

186 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 85, NO. 3


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lungs. The inferior vena cava, aorta, and portal veinwere tied off to keep the lymphatic drainage intact. A31-ga needle was inserted into the lymphatics along theedge of the liver margin, liver capsule, gallbladder, andthe portal vein. A 10-mL syringe was used to handinject saline and Ethiodol oil (Savage Laboratories,Melville, New York) into the lymphatics of the liver.This same technique was used by the senior author(JDC) on the resected bowel of four adult white rats andrabbits to determine the time for anastomosis of thesevered lymphatics in small bowel transplantationexperiments.

Normal saline was injected selectively into themarginal lymphatics to identify the largest lymphchannels for cannulation. The capsular, marginal,gallbladder, and portal vein lymphatics were cannu-lated. The needles were then connected with K-50tubing to a 20-cc plastic syringe. The Ethiodol oil wasinfused by hand. Overhead and spot fluoroscopic filmswere obtained using a Phillips radiographic fluoro-scopic unit (Phillips Medical Systems, Hamburg,Germany). A Picker P-Q 2000 (Picker International,Cleveland, Ohio) scanner was used to obtain the

transverse (axial) CT images. A multiplane reconstruc-tion program was used to obtain the sagittal and coronalCT images. The liver was placed into a cardboard boxto secure it in a fixed position. The box was insertedinto the CT gantry and oriented to obtain the coronaland sagittal images.A 1.5 Telsa GE Signa MRI unit (GE Medical

Systems, Milwaukee, Wisconsin) was used to obtainTI-weighted coronal and transverse images. Threedimensional reconstructed color images were providedby ISG Technologies (ISG Technologies Inc, Missis-sauga, Ontario, Canada). Four bags of 500 mL normalsaline solution were placed beneath the fresh liverspecimen to enhance the image quality. Ektachrome100 daylight film was used to obtain color slides for thefigures.

RESULTSThe heart, lungs, and liver were harvested from 15

swine within 20 minutes following euthanasia. Thesurface of the lungs were very red from the pooling ofblood in the capillary bed. The harvested liver was notdiscolored (Figure 1). The glistening lymphatics of the



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Figuren . A2e D reconstructed CT image of theswine liver in a cardboard box demonstratingthe cursor lines numbering the coronal imcages.

liver, gallbladder, portal vein (Figure 2), and inferior cavawcolaeralvedayptas the visceral pleural lymphatics ofthe lung. The multiple benzene-like structures of thehepatic lobules were clearly identified on the liver surface(Figure 3).

Retrograde saline injections into the marginal andcapsular lymphatics over the liver surface demonstratedthe collateral lymphatics along the liver edge (Figure 4).The needles were introduced but not secured in thelymphatics over the liver surface because the lymphaticswere contiguous with one surface of the liver (Figure 5).T'he injection (antegrade) into the surface lymphatics ofthe gallbladder dilated and demonstrated intrahepaticcollateral lymphatics and lymphatics marginating theportal vein (Figures 5, 6, and 7). The surgical dissectingscope confirmed the narrowed constricted areas as valvesin the lvmphatics draining the gallbladder. The surface

-~~~~~~

Figure 9. A 2.D reconstructed CT image of theswine liver in the coronal plane. Intrahepaticand interlobular lymphatics are filled with oilycontrast (white arrows). Capsular lymphaticsare indicated by the black arrows.

lymphatics dilated at the tip of the needle from 1 mm to1.5 mm (Figure 5). The saline injections allowed our teamto select several lymphatics for cannulation. Salineextravasated at the injection sites of the untied lymphat-ics. The large surface lymphatics of the gallbladder weredissected free of the gallbladder, and the inserted needlewas tied in place easily. The cannulation of thelymphatics along the liver edge and the portal vein provedto be the most difficult because the needles were largerthan the lymphatics.

The injection of Ethiodol was difficult because theviscosity of the oil added to the opposing pressure of thesmaller intrahepatic and marginal lymphatics. Thecontinued contrast injections in the capsular lymphaticsdemonstrated contrast at the surface of the liver and inthe lymphatics marginating the inferior vena cava,portal vein, and the gallbladder (Figure 7). Computer-ized tomographic coronal and 2-D reconstructionimages documented collateral flow between the smoothsurface capsular lymphatics, intrahepatic, and visceralinterlobular lymphatics (Figures 8 and 9). Magneticresonance images and plain radiographs confirmed thesaline and contrast injections. The reconstructed 2-DCT (Figures 8 and 9) and 3-D MR images (Figures 10and 11) best demonstrated collateral circulation be-tween the visceral (smooth) surface lymphatics and theinterlobular lymphatics (Figures 5 and 6). Magneticresonance imaging documented the oily contrast in theperiportal lymphatics and not within the hepatic veins.

DISCUSSIONA knowledge of the hepatic anatomy is mandatory



Figure 10. A coronal MR image demonstratingthe periportal lymphatics (black arrows), mar-ginal lymphatics (white arrow), portahepatis(PH), and hepatic veins (V).

for the performance of liver transplantation. Thevascular anatomy of the liver has been reviewedextensively in anatomy textbooks and in scientificarticles.4 However, the anatomy of the hepatic andadjacent lymphatics has not been extensively re-searched for purposes of improving transplantation.A literature search did not reveal any articles on the

visual and direct cannulation of the surface lymphaticsof the liver. However, collateral lymph circulation canbe demonstrated and does occur in the upper and lowerextremities.5 Collateral circulation does exist within theliver and the lung and has been demonstrated by suchauthors as Burgener et a16 in 1977, Deimer7 in 1983, Itoiet a18 in 1988, and Collins et all in 1991. Thelymphatics of the liver and the lung can be cannulatedwith large-bore modified Viamonte 18-ga blunt tipneedles. The surface lung and hepatic lymphaticanatomy in swine and human lymphatics have a similardistribution. The imaging of the liver and lunglymphatics in the swine model is currently being usedto further the teaching of anatomy to residents inradiology and at autopsy rounds in pathology.1

Plain radiography, CT, and MRI can demonstrate thecommunication of the contrast-filled liver lymphaticswithin the portahepatis. Computerized tomographydemonstrates contrast in the intrahepatic collateral

Figure 11. A 3-D reconstructed transparentcolor MR image of the liver demonstrating theoverlay filling of many intrahepatic lymphat-ics. Oily contrast exits from the cut lymphat-ics at the portahepatis (PH). Periportal andinterlobular lymphatics are indicated by thearrows.

lymphatics, and the 2-D reconstructed CT images bestdefine periportal and perivascular lymphatic collateralcommunication. Therefore, the ligamentous attach-ments of the liver become very important in performingliver resections and transplantations.

Briefly, the human liver has four segments and theswine liver has four lobes. The larger human liver isconnected to the undersurface of the diaphragm and tothe anterior wall of the abdomen by five ligaments. Fourof these are peritoneal folds (falciform, coronary, andtwo triangular lateral ligaments). The fifth is the roundligament (the fibrous cord of the obliterated umbilicalvein). Within these ligamentous fascia planes andconnective tissue are lymphatics, small blood vessels,and nerves. The human liver is further fixed in theabdomen by the ligaments, connective tissue, inferiorvena cava, and the hepatic veins. The falciformligament does not contribute to the support of the liver.7Our dissections of the swine liver reveal that the rightdome of the liver is connected by a thin circularligament (containing lymphatics, veins, and capillar-ies). Further communication with the diaphragm isestablished at the inferior vena cava hiatus, portahepatis(Figure 1), and the surrounding peritoneal folds of theadjacent bowel and vascular structures. Swine lymphat-ics also anastomose the undersurface of the diaphragm



...

Figure 12. Drawing of the swine liver as itappears grossly after harvesting. The smoothdorsal surface is anterior, and the right lobe ofthe liver is on the right. The liver is notattached to the dome of the diaphragm. Thecapsular lymphatics are seen enlarged withinthe circle.

Figure 13. Drawing of the swine liver dem-onstrating the 3.D appearance of the capsularlymphatics communicating with surface, mar-ginal, portal, biliary, and hilar lymphatics. Thepolygonal hepatic lobule is enlarged in theupper left corner.

to the hepatic veins and the inferior vena cava.The review of our surgical operative reports indicate

that the lymphatics are not tied or stented in liver andlung resections or cardiac transplantations. Large rightpleural effusions and ascites are common postoperativecomplications in liver transplantations and are routinelydemonstrated on the postoperative upright chest andabdominal radiographs. When the liver is removed fromthe recipient, the lymphatics are transected and notligated. The transplanted liver is secured to the

recpient's vasclrsuplyandeintvestinal aTtahe ments.

Pulmonary Lymphatica

Pulmonary ligamentThoradc Duct

Diaphragmliver-

Gisterna Chyli

Portal Lymphatics

Figure 14. Diagram demonstrating the com-munication between the liver, abdomen, dia-phragm, and lung. The portal lymphatics anas-tomose within the liver. The pulmonarylymphatics in the pulmonary ligament arecontiguous with the diaphragm via the vis-ceral pleura.

The lymphatics remain unattached. The severed lym-phatics connecting the liver to the visceral surface of thediaphragm and visceral pleura of the lung are free todeposit lymph. The lymph leaks from the unattachedlymphatics resulting in postoperative pleural effusions,ascites, and loss of electrolytes. This has led topostoperative accumulation of free fluid interferingwith lung aeration and pneumonias because the lym-phatics had been overlooked intraoperatively.

Surgery performed on large adult rats and whiterabbits by the senior author (JDC) determined that thelymphatics were fully reunited without cannulation in10 to 14 days postsurgery. The injection of oily contrast(Ethiodol) documented that the lymphatics were intact.It would seem logical that stenting or anastomosingsome of the major hepatic lymphatics would reducepostoperative complications.

The surface or capsular lymphatics of the swine liver(Figures 3 and 4) communicate with the polygonalhepatic lobules and appear as continuous strands ofbenzene ring (Figure 12). The lymphatics intercommu-nicate with marginal surface lymphatics as collateralsleading to an elevator shaft in a tall building (Figure13). They anastomose with the portal, biliary, andhepatic vein lymphatics (Figures 13 and 14).

The studies by Deimer7 illustrated the communicationof the surface lymphatics (marginal) with intrahepaticlymphatics (Figures 13 and 14). We were not able todocument extravasation of lymph from a stroma assuggested by Deimer.7 We did observe collateral fillingof the lymphatics of the diaphragm communicating with



the lungs. Figure 14 is a modified diagram from a studyby Deimer that demonstrates the communication of theportal lymphatics within the liver.7 The human and swineliver lymphatics anastomose with the lymphatics of theinferior cava, diaphragm, lung, and thoracic duct. In theswine, the pulmonary lymphatics anastomose at thesuperior aspect of the diaphragm by a circular ligament asdescribed and as the inferior vena cava enters the thorax.

Autopsies on liver transplant patients at our institutiondemonstrate passively congested enlarged livers. Thecapsular (surface) lymphatics and marginal lymphaticsare dilated and grossly visible. Swabbing the liver surfacewith methylene blue selectively identifies the dilatedlymphatics. Obstruction of the lymphatics does not allownormal lymph flow from the hepatic lobule into the portaltriad. It is reasonable to assume that the same metaplasticchanges occur in the liver when the lymphatic drainage isnot reestablished. Collateral lymphatic circulation is ableto drain some hepatic lymphatics (circumvention) incases of injury to liver cords. However, if there are noestablished sizable lymphatics to drain the hepatic lobule,the common bile duct and hepatic veins can onlyaccommodate lymph drainage for a given time. Becausethe gallbladder is removed at liver transplantation, thelargest lymphatic over the gallbladder could be selectedfor a stent or tubing, which may assist in the reduction ofthe edematous changes often accompanying transplanta-tion. We intend to pursue our research to evaluate thishypothesis.

AcknowledgmentThe authors thank Randy C. Duke for his help with computer

graphics.

Literature Cited1. Collins JD, Shaver ML, Disher AC, Batra P, Brown K,

Miller TQ. Imaging the thoracic lymphatics: experimentalstudies of swine. Clinical Anatomy. 1991;4:443-446.

2. Collins JD, Disher AC, Shaver ML, Miller TQ. Anatomy ofthe lymphatic drainage of the liver as displayed by the plainx-ray and magnetic resonance imaging. Anat Rec.1991;228:17A. Abstract.

3. Koslin DB, Stanley RT, Berland LL, Shin MS, Dalton SC.Hepatic perivascular lymphedema: CT appearance. AJR Am JRoentgenol. 1988;150:111-113.

4. Ger R. Surgical anatomy of hepatic venous system.Clinical Anatomy. 1988;1 15-22.

5. Collins JD, Bassett LW, Snow H, Ross NA, Patin T.False positive thromboscintigram resulting from lymphedema: aroentgen pathological model. J Natl Med Assoc. 1986;78:875-881.

6. Burgener FA, Webber DA, Kormano M. Hepatographyand liver lymphography by retrograde biliary ethiodol infusion:an experimental study in the dog. Invest Radiol. 1977;12:259-266.

7. Deimer EE. Clinical Radiology of the Liver New York,NY: Dekker; 1983.

8. Itoh T, Kanaoka M, Obara A, Furuta M, Itoh H.Lymphangiosis carcinomatosa of the liver. Acta Pathol Jpn.1 988;38:751 -758.

9. Gray H, ed. Anatomy of the Human Body. 27th ed.Philadelphia, Pa: Lea & Febiger; 1959:1300-1301.

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IMAGING THE HEPATIC LYMPHATICS: EXPERIMENTAL STUDIES …€¦ · IMAGINGTHEHEPATIC LYMPHATICS:EXPERIMENTAL STUDIESINSWINE JamesD. Collins, MD,Anthony C. Disher, MD, Maria L. Shaver,