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1990, The British Journal of Radiology, 63, 26-30Ultrasound examination of lymph nodes in the hepatoduodenal ligamentBy *K. Lyttkens, MD, L. Forsberg, MD, PhD and E. Hederstrom, MD, PhDDepartment of Diagnostic Radiology, University Hospital, S-221 85 Lund, Sweden(Received May 1989 and in revised form August 1989)

Abstract . Ninety patients, found to have lymph nodes in the hepato-duodenal l igament (HDL) on ultrasound examination werereviewed over a one-year period in order to define the diseases in which such nodes can be found. The patients were divided intofour ma in g roup s: benign liver disease ( = 31), malignan t disease ( = 26), disease of the gallbladder or the biliary tree (= 14) anda group with various benign, most inflammatory diseases (n = 19). In 40% of the patients (36/90), the lymph nodes in the HDLwere the only sign of disease on ultrasound examination, and the majority of those were in the benign group.

Patients with abnormal liver function tests or upperabdominal pain are often examined initially with ultra-sound. A changed echo pattern of the liver with fattyinfiltration can usually be detected (Taylor et al, 1976;Foster et al, 1980), whereas to diagnose mild cirrhosiswithout fatty infiltration and chronic active hepatitisand related diseases is often difficult or impossible(Dewbury & Clark, 1979). The finding of abnormallymph nodes in the hepato-duodenal l igament (HDL)might, however, indicate the presence of liver diseaseand detection of nodes in the HDL by ultrasound isfeasible (Fo rsberg & He ders trom , 1985; Fors berg et al,1987).

The nodes surrounding the hepatic artery ventral tothe portal vein are generally those observed, but nodescan also be seen dorsal to the portal vein. Nodes in theHDL in chronic active hepatitis have been reported oncomputed tomography (CT) (Gore et al , 1988). Lymphnodes in the HDL can be seen in patients with benign aswell as malignant diseases (Baker et al, 1987; Heder-strom & Forsberg, 1987): in anatomical atlases they arecalled hepatic nodes and drain mainly the hepato-biliarysystem. In this study, however, lymph nodes were notedin patients with diseases of other organs as well, indi-cating lymph drainage to the nodes in the HDL, directlyor indirectly. The aim of this review was to define thosediseases in which nodes in the HDL can be detected byultrasound.Material and methodsThe study covered 90 consecutive patients, 63 femaleand 27 male, with a mean age of 56 years (range4-91 years), examined over a one-year period, in whomnodes (>0.5cm) were observed in the HDL on ultra-sound examination. All patients were examined withdynamic ultrasound using 3.5 MH z and 5 MH zmechanic sector scan transducers and all the examina-tions were performed by radiologists with extensiveexperience in ultrasound. Most patients had beenfasting for 4 to 12 h before the exam inati on. Th e*Author for correspondence.

echogenicity and the homogeneity of the liver paren-chyma and the size and echogenicity of the lymph nodesin the HDL were registered. The nodes were sometimesflattened or oval in shape, in which case the largestmeasurements were noted. Measured in retrospect, thenodes were subdivided into four groups according tosize (Table I).Follow-u p of 6 month s (deceased patients) to 3 yearslater was made by studying case records. Histopatholo-gical diagnosis was available from autopsy in six cases,and from biopsy or surge ry in 50 cases. In the rem aining34 cases the final diagnosis w as obta ined from clinicalfindings, including liver function tests (serum bilirubin,alkaline phosphatase, aminotransferase and y-glutamyl-transferase) and radiological examinations.

The patients were divided into four main groupsdepe nding on diagno sis: ben ign liver disease ( = 31),malignant disease (n = 26), disease of the gallbladder orthe biliary tree (n 14) and a group of miscellaneousdiseases (= 19). A patient who had a gallstone or hadhad a cholecystectomy was classified as having gall-bladder disease, since we noted that the nodes in theHDL seen in patients with cholecystitis do not seem todisappear after cholecystectomy.Malignant disease overrode the diagnosis of benigndisease.ResultsBenign liver diseaseThis was found in 31 patients (Table II). A histo-logical diagnosis was available for 25 of these and thefinal diagnosis was established from clinical findings insix cases.Table I. Lymph nodes in the hepato-duodenal ligamentSize of node(cm) G r o u p Size of node(cm)

1.01.52.0


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Ultrasound of lymph nodes in the hepato-duodenal ligamentTable II. Benign liver disease (31 patients)

Nu mb er of Ultra sou nd of the liver Liver testspatientsLymph nodes

Normal Abnormal Normal Abnormal I II III IVHepatitisHepatopathyCirrhosisDrug side-effect

135112

7461

6151

Total 31 18 13

13511231

112

423110

1146

82313

All the patients had abnormal liver function tests, andin most cases the levels were seriously abnormal.Thirteen patients had an abnormal echo pattern ofthe liver parenchyma: grossly irregular liver structure insix cases, increased echogenicity of the parenchyma infour cases (as is often seen with fatty infiltration) anddecreased echogenicity in three cases.Among the 13 patients with hepatitis, eight had nodes^2.0 cm. The other three subgroups showed irregularityin size of the nodes.Malignant diseaseThis was found in 26 patients, with a histologicaldiagnosis available for 24 cases. The final diagnosis wasmade from a radiological examination in two cases(Table III).Twenty patients had abnormal liver function tests,four were normal and in two cases no tests wereavailable.

In three patients the liver parenchyma could not beevaluated because of bowel gas in two patients anddilated biliary ducts in one patient. An abnormal echopattern of the liver was found in 15 patients: the liverstructure was irregular owing to malignant infiltrationin 12 cases and non-malignant causes in one case; theechogenicity was increased in one case and decreased inone case.

Eight patients had a normal echo pattern of the liver:the ultrasound examination showed a tumour of thepancreas in one of these patients; a patient with chroniclymphocytic leukemia had a considerably enlargedspleen and two patients with ovarian tumours hadascites.All patients except one had lymph nodes that were1.0 cm or larger. Of these, half (n 13) had nodes of atleast 2.0 cm, and the other half (=12) had nodesbetween 1.0 cm and 2.0 cm.

Disease of the gallbladder or the biliary treeSuch disease was found in 14 patients (Table IV),histologically confirmed in eight cases. Final diagnosiswas made from clinical findings in six cases.One patient with previous cholecystectomy hadnormal liver function tests, and the remaining 13patients had abnormal tests. Abnormal echogenicity ofthe liver was observed in five patients; irregular liverstructure in two cases; increased echogenicity in twocases and decreased echogenicity in one case.Ultrasound showed normal liver parenchyma in ninepatients: five of these had gallstones or dilated bileducts.The size of the nodes in the different subgroups wasirregularly distributed.

Table III. Malignant disease (26 patients)

Liver metastasesCarcinoma of the gastro-intestinal tract andpancreatic carcinoma,without liver metastasesLymphatic malignancyOvarian tumourHypernephromaCarcinoma of the lungTota l

Vol. 63, No. 745

Numberpatients

13

6321126

of

32218

Ultrasound of the l iverNorma l

1

1

13

No results Abn ormalavailable12

21

15

Liver testsNorm al No resultsavailable

2 111 1

4 2

Abnorma l

13

3211

20

LymphI II

4

31111 9

nodesIII

2

1

3

IV

7

221113

27


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K. Lyttkens, L. Forsberg and E. HederstromTable IV. Disease of the gallbladder or biliary tree (14 patients)

Cholangitis/cholecystitisCholecysto-/docholithiasisPrevious cholecystectomyTotal

Number ofpatients

662

14

Ultrasound of the liverNorma l4419

Abnorma l2215

Liver testsNorma l

11

Abnorma l661

13

Lymph nodesI

11

II1214

II I3216

IV213

Benign, mostly inflammatory diseasesThese were found in 19 patients (Table V), confirmedhistologically in four cases and by clinical examinationin 15 cases.Liver function tests were normal in eight patients andabnormal in 11. An abnormal echo pattern of the liverwas found in four cases: irregular in one patient,increased echogenicity in one and decreased echogeni-city in two patients.For the majority of patients (n = 15), ultrasoundexamination showed normal liver parenchyma; five ofthese had pancreatitis. Even in this group of miscella-neous diseases, the size of the lymph nodes variedconsiderably.DiscussionIn the abdomen, the term "ligament" refers to a foldof peritoneum supporting any of the abdominal viscera.A peritoneal ligament consists of two layers of perito-neal membrane and the mesodermal tissue, bloodvessels and lymphatic structures enclosed between thetwo layers. The stomach is entirely covered with perito-neum. A double layer of peritoneum, the lesseromentum, includes the hepato-gastric ligamentextending from the ligamentum venosum of the liver tothe lesser curvature of the stomach, and the HDLpassing from the porta hepatis to the pyloric region andthe upper horizontal portion of the duodenum. The freeedge of the HDL, through which run the portal vein, thehepatic artery, the common bile duct and the hepaticlymph vessels, forms the ventral margin of the epiploic

foramen (foramen of Winslow), which gives access tothe lesser peritoneal sac (bursa omentalis) (Netter, 1979;Balfe et al, 1984; Weill et al, 1986).The lower third of the oesophagus, the gastric wall,the duodenum, the small intestine and the proximalportion of the large intestine drain partly into thecoeliac (middle supra-pancreatic) nodes, which aresituated above the pancreas and around the coeliacartery and its branches. The pancreas also drains intothe coeliac nodes and to the chain of hepatic nodesalong the bile ducts. The lymph from the liver, thegallbladder and from most of the extrahepatic bile ductsdrain into the hepatic lymph nodes around the commonbile duct and the main stem of the portal vein. Thelymphatic vessels continue to the chain of coeliac nodes(Netter, 1979).Since the vast majority of patients do not routinelyshow any lymph nodes in the HDL (Fig. 1), one canassume that normal hepatic nodes cannot be visualizedby ultrasound. One explanation might be that they areboth small (< 0 .5 cm) and have an echogenicity of aboutthe same level as the surrounding fat. Nodes associatedwith inflammatory or malignant disease becomeenlarged or display decreased echogenicity. Lymphnodes, even of small size, with an echopoor appearancemight indicate disease.Abnormal lymph nodes in the HDL are usuallyrounded or oval and can often be distinguished fromeach other by the fat and connective tissue preservedbetween the nodes. When echopoor lymph node aggre-gations are present in the HDL, the hepatic artery

Table V. Miscellaneous diseases (19 patients)

Gastri t is/duodenitis/peptic ulcerPancreatitisColitisSalmonella paratyphi sepsisAmoebic dysenteryCollagen diseaseTota l

Number ofpatients

66321119

Ultrasound of the liverNorma l

65211

15

Abnorma l

112

4

Liver testsNorma l321118

Abnorma l34211

11

Lymph nodesI

11

2

II34

7

III211

15

IV12115

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Ultrasound of lymph nodes in the hepato-duodenal ligament

Figure 1. Longitudinal scan through normal hepato-duodenalligament. The hepatic artery (arrow) is surrounded by fat.

acquires a very bright delineation creating the appear-ance of a halo around the artery when scanned transver-sely (Fig. 2).The proximity to the duodenal bulb, together withobscuring gas, sometimes m ake the ultrasonic visualiza-tion difficult. Examining the patient in a sitting positionmay be helpful. The skill and experience of the ultraso-nographer is of decisive importance for the detection oflymph nodes in the HDL.The absolute size of the lymph node seems to be ofminor importance in most cases. We noted a consider-able variation in the size of the lymph nodes in thevarious groups of diseases. In the malignant group, 50%(13/26) of the lymph nodes were less than 2 cm, and thiswas also the case in 67% (43/64) of the nodes in thebenign group. This is in agreement with the review ofabdominal lym phadenopathy in benign disease detectedby CT by D eutch et al (1987) who found that the size oflymph nodes is not useful to differentiate benign frommalignant processes. Patients react differently withregard to the degree of node enlargement and change innode echogenicity, independent of the underlyingdisease. Not every patient with acute hepatitis, forinstance, has enlarged lymph nodes in the HDL. Ifnodes are present, their size shows a substantial varia-tion from one patient to another. Possibly there is achange in the size of lymph nodes during the course of adisease (Gore et al, 1988).Extensive abdominal lymphadenopathy is most oftencaused by lymphoma and metastatic disease, but canalso be observed in a number of benign entities. Lymphnodes respond to a variety of external stimuli, includinginflammatory, infectious, systemic and immunologicdisorders, as well as malignant processes (Deutch et al,1987).The lymph nodes of the HDL, especially thosesituated close to the hepatic artery, seem to be involvednot only in diseases of the biliary tract and in wide-spread malignant disease but also directly or indirectlyin inflammatory diseases of the gastro-intestinal tract.

Figure 2. Oblique scan along portal vein-splenic vein (arrow-head). Irregular liverparenchyma owing to metastases. (a) A"h alo " around the hepatic artery (small arrow) and an enlargedlymph node (large arrow) caudal to the artery and d orsal to theliver, (b) The hepatic artery (small arrow) is surrounded by twolarge lymph nodes (large arrows).

This finding is supported well by our knowledge of thecomplex lymphatic system in this region.In this study about one third of the patients (26/90)had malignant disease causing lymph node enlargementin the HDL, whereas Deutch et al (1987) found malig-nant disease causing abdominal lymph node enlarge-ment in 94% of the patients on CT. Our material,however, consists only of patients with lymph nodes inthe HDL, whereas Deutch's material included abdo-minal lymphadenopathy in general. As described byBaker et al (1987), the HDL is difficult to evaluate usingaxial CT because of its oblique orientation, anatomicVol. 63, No. 745 29


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K. Lyttkens, L. Forsberg and E. Hederstromvariability, paucity of fat and compact volume. Sinceultrasound has the advantage of unlimited scan planes,it may show a small periportal abnormality with morecertainty than CT, especially in a patient with a thinbody habitus.More than half of the patients with benign liverdisease (18/31) ha d lymph nodes in the HDL as the onlysign of disease on ultrasound examination. Thiscompares favourably with previous work by Forsberg etal (1987, 1985), who have shown that ultrasonic visuali-zation of lymph nodes in the HDL seems to increase thepossibility of detecting early diffuse liver disease evenwhen the liver parenchyma appears sonographicallynormal.Only a few (4/26) patients in the malignant grouppresented with lymph nodes in the H DL as the only signof disease on ultrasound scans, while half of those in thebenign group did so (32/64).It is well known that malignancies which metastasizeby means of the lymphatics cause enlargement ofregional as well as distant lymph nodes. In the malig-nant group in our material, the tumour was located inthe abdomen in 22 of the 26 cases.Most of the patients in the biliary group (10/14)presented with other signs of disease, such as abnormalechogenicity of the liver parenchyma, gallstones ordilated biliary ducts which are sonographically easilydetectable, and it is reasonable to assume, because of theanatomy, that disease of the gallbladder and the biliarytree, as well as benign liver disease, may cause changesin echogenicity and size of the lymph nodes in the HDL(Forsberg & Hederstrom, 1985; Deutch et al, 1987;Forsberg et al, 1987; Hederstrom & Forsberg, 1987;Gore et al, 1988).About a quarter (19/90) of the patients in our studyhad a disease that was neither malignant nor located inthe hepato-biliary tract. Twelve patients had inflamma-tory or infectious disease of the gastro-intestinal tract;the pancreas was involved in six cases and there was onecase of collagenosis. Half of the patients (10/19) in themiscellaneous group had no other sign of disease thanthe lymph nodes in the HDL, which accords with thelimited ability to detect inflammatory gastro-intestinaldisease with ultrasound. A possible, indirect way thatthe lymph nodes in the HDL may be affected is by theblood flow from the gastro-intestinal tract through theportal vein to the liver, since the lymphatics from theliver drain into the lymph nodes in the HDL. In thisway, lymph nodes in the HDL might indicate boweldisease.In 50 patients with no rmal liver parenchyma on ultra-sound examination, the lymph nodes in the HDL indi-cated disease in the upper abdom en. Of these, there werefour patients in the group of malignant diseases, fivepatients in the biliary group and five patients in the

group of miscellaneous diseases with other pathologicalfindings on ultrasound examination. Thus in 40% of thepatients (36/90), the nodes in the HDL were the onlysonographic sign of disease.Sometimes lymph nodes in the HDL are the onlyfinding observed on ultrasound examination in a patientwith abdominal pain, indicating that further investi-gation and follow-up should be considered. Nodes inthe HDL might indicate inflammatory disease of theabdomen, and could be a parameter with which tofollow the course of disease during treatment. Furtherstudies of this group of patients without malignancy orhepato-biliary disease are warranted.

ReferencesBAKER, M. E., SILVERMAN, P. M., HALVORSEN, R. A. & CO H A N ,R. H., 1987. Computed tomography of masses in periportal/hepatoduodenal l igament. Journal of Computer AssistedTomography, 11, 258-263.BALFE, D. M., M A U R O , M. A., KOEHLER, R. E., LEE, J. K. T.,W E Y M A N , P.J., Picus, D. & PETERSON, R. R., 1984.Gastrohepatic l igament: normal and pathologic CTanatomy. Radiology, 150, 485-490.D E U T C H , S. J., SANDLER, M. A. & A L P E RN , M. B., 1987.Abdominal lymphadenopathy in benign diseases: CTdetection. Radiology, 163, 335-338.D E W BU RY , K. C. & C L A R K , B., 1979. The accuracy ofultrasound in the detection of cirrhosis of the liver. BritishJournal of Radiology, 52, 945-948.FORSBERG, L., F L O RE N , C. H., HEDERSTROM, E. & P RY T Z , H.,1987. Ultrasound examination in diffuse liver disease.Clinical significance of enlarged lymph nodes in the hepato-duodenal l igament. Ada Radiologica, 28, 281-284.FORSBERG, L. & HEDERSTROM, E., 1985. The lymph nodes of

the hepatoduodenal l igament in non-malignant hepatobil iarydisease. Journal of Ultrasound in Medicine and Biology,Supplement No. 1, p. 86.FOSTER, K. J., D E W BU RY , K. C , G RIF F IT H , A. H. & W R I G H T ,K., 1980. The accuracy of ultrasound in the detection of fattyinfiltration of the liver. British Journal of Radiology, 53,440^442.G O R E , R. M., VOGELZANG, R. L. & N E M CE K , A., 1988.Lymphadenopathy in chronic active hepatitis: CTobservations. American Journal of Roentgenology, 151,75-78.HEDERSTROM, E. & FORSBERG, L., 1987. Ultrasonography incarcinoma of the gallbladder. Acta Radiologica, 28, 715-718.NETTER, F. H., 1979. The CIBA collection of medicalillustrations, Vol. 3, Digestive system, Parts I-III, (CIBA

Pharmaceutical Company, London).TAYLOR, K. J. W., CARPENTER, D. A., H I L L , C. R. &

MCCREADY, V. R., 1976. Gray scale ultrasound imaging.The anatomy an d pathology of the liver. Radiology, 119,4 1 5 ^ 2 3 .W E I L L , F ., W A T R I N , J., RO H M E R, P., W E IL E R, S. & CO CH E , G.,1986. Ultrasound and CT of peritoneal recesses andligaments: a pictorial essay. Ultrasound in Medicine &Biology, Vol. 12, No. 12 , 977-989.

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