Clin. Radiol. (1977) 28, 653-658

T H E L Y M P H O G R A M IN A B D O M I N A L T U B E R C U L O S I S

C. A. BEETLESTONE,* W. WIELAND,* E. A. LEWIS? and S. O. ITAYEMI+

*Department of Radiology, University College Hospital, Ibadan, Nigeria, ?Department of Medicine, University College Hospital. Ibadan, Nigeria, +Department of Surgery, University College Hospital, Ibadan, Nigeria

Lymphograms of 11 patients with histologically proven abdominal tuberculosis have been assessed in an attempt to define a typical pattern of appearance in retroperitoneal lymph glands. Glandular enlargement, poor glandular filling and lymphovascular obstruction were present. A gradient of abnormality with more marked adenopathy in the upper para-aortic chain extending to a lesser involvement below in the iliac chain was demonstrated in keeping with a retrograde spread of the tuberculosis process from the abdominallymphatics cauded along the retroperitoneal chain. Lymphography may be valuable in cases where data from clinical observations and routine radiological studies is inconclusive in cases of vague abdominal disease.

INTRODUCTION

The diagnosis of abdominal tuberculosis remains a clinical problem. The insidious onset of symptoms, their protean nature, non-specific physical findings (often without parenchymal lung pathology), and a lack of specific diagnostic tests short of a laparotomy all lead to uncertainty.

The study was started with the express purpose of investigating the value of lymphography as a diag- nostic tool in suspected cases of abdominal tuber- culosis.

MATERIAL

Twenty-five patients with suspected tuberculosis of the abdomen at University College Hospital (UCH), Ibadan, Nigeria, underwent lymphography during 1973 and 1974. Eleven cases in which a definite histological diagnosis of tubercle was estab- lished are reviewed here. Lymphograms of 15 patients with no evidence of tuberculosis were used as controls.

METHODS

Patients underwent our routine radiological evaluation for suspected cases of abdominal tuber- culosis, including chest and abdominal films, barium enema, barium meal and follow-through using a non-flocculable barium.

Standard bipedal lymphograms were performed. A total of 10-15 ml of Lipoidal Ultra Fluid (May & Baker Ltd, Dagenham, England) was injected. Films were taken during injection and again 24 h after the lymph nodes were filled. The four standard positions

to demonstrate retroperitoneal nodes were used (AP supine, right and left supine obliques and a left lateral) to permit projection of the lymphatics free of the vertebral bodies and to minimise superimposition of glands.

Glandular enlargement was noted. The pattern of falling defects in the individual nodes was assessed. These defects were classified by radiographic appear- ances according to the site of involvement (marginal or central) and whether they were ill defined or well defined. The degree of replacement was assessed subjectively from 1 + (minimal defects) to 4+ (com- plete glandular replacement). Lymphovascular ob- struction was assumed to be present when any of the following were present (i) extensive lack of filling of the para-aortic nodes; (ii) stasis in large deformed lymphatic channels; (iii) abnormal lymphovenous shunts; and (iv) collateral channels.

RESULTS

The 11 patients in the study included five males and six females between 15 and 40 years.

Clinical Features. - All patients presented with a history of abdominal discomfort and progressive weight loss. Pyrexia was present in three cases. There were palpable glands in only two patients. Five had clinical ascites while three others had tender central abdominal masses.

Diagnosis.- Biopsy material, obtained at laparo-- tomy in nine cases and from peripheral glands in two cases, showed positive histological findings of tuber- culosis.

Control Subjec ts . - Fifteen controls had no evi- dence of tuberculosis. Some of these patients showed

654 C L I N I C A L R A D I O L O G Y

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THE LYMPHOGRAM IN ABDOMINAL TUBERCULOSIS

Table 2a - Lymphadenographic findings in tuberculosis of the abdomen

655

Case Enlargement of Primary nodes

Filling defects in primary nodes

Predominant site of defects

Definition of defects Degree of node replacement (ex ten t of defects)

1 No Marginal Poor +++ 2 Yes Central Poor ++ 3 Yes Central ~ marginal Poor ++++ 4 Yes Central ~ marginal Good ++++ 5 Yes Central Good ++++ 6 Yes Marginal ~ central Poor +++ 7 Yes Central ~ Marginal Good +++ 8 No Central ~ Marginal Good +++ 9 No Maxginal Good +

10 Yes Marginal Poor + 11 No Marginal > Central Good ++

Table 2b - Evidence of Obstruction in the Lymphogram

Case Obstruction Gradient of abnormality

Collateral formation Other signs of obstructions

Enlargement of collateral nodes

Enlargement of collateral channels

1 No No Stasis 3 2 No No Stasis 2 3 Yes Yes Stasis 3 4 Yes Yes Stasis,

varicosity 3 5 No Yes Stasis,

dilatation 1 6 No No Stasis 2 7 No No None 1 8 No No None 2 9 No No Dilatation 2

10 No No None 2 11 No Yes Stasis 2

minor abnormali t ies in the inguinal l y mp h nodes, In three cases, (nos. 2, 5, 7 and 10) plain histologically a non-specific peripheral adenitis was abdomina l films were .negative bu t there were ab- present, normali t ies on the bar ium studies. Radiology - General Features One case (no. 4) showed no abnormali t ies on the

Chest Films (Table 1) - Eight pat ients had normal plain film nor on bar ium studies. chest films. One had a pleural effusion and two Lymphograph ic F i n d i n g s - F o u r dist inct ab- showed upper lobe infiltrates characteristic o f adult normal appearances affected the individual nodes of tubercle.

Abdominal Radiological F ind ings - Plain Films and Barium Studies (Table 1) - In 9 cases out of 11 (nos. 1. 3, 6, 8, 9 and 11) the appearances of the plain fdm and bar ium studies were suggestive of moderate to severe in t ra-adbominal lesions. Ascites, je junal oedema, rigid small bowel loops, soft tissue masses and obs t ruc t ion were present.

the peri toneal chain (Table 2a, b)

(1) Glandular enlargement (2) Poor glandular filling (3) Lymphovascular obs t ruc t ion (4) Gradient o f abnormali t ies

(a) Poor filling (b) Glandular enlargement

656 C L I N I C A L R A D I O L O G Y

Fig. 1 - T h e number of filled aortic glands is particularly sparse. Any drainage pattern in the upper aortic area is hardly detectable, but nevertheless, drainage into the distally stenosed thoracic duct does ultimately occur. A lympho- venous shunt is demonstrated, oily contrast globules are seen on either side of the upper lumbar area (note residual barium in appendix).

Glandular Enlargement. - In 7 cases out o f 11 the pr imary modes were enlarged (Table 2a). The uptake pat tern of the contrast was basically that of in f lammat ion .

Poor Glandular Filling. - All of our cases showed some filling defects. Failure of contras t uptake, due to varying degrees of glandular replacement , was manifest lymphographical ly as a spec t rum ranging from minimal ill-defined filling defects (Fig. 2), to complete replacement of m a n y nodes (Fig. 1, 3, 4). The subjective degree of node rep lacement or ex ten t o f filling defects is charted in Table 2a. In six cases the defects were well defined as i l lustrated in Fig. 5. In five cases they were no t so clear-cut.

Defects were located bo th marginal ly and cen- trally. In six cases there was a comb ina t i on of b o t h (Table 2a). In three cases the defects were main ly marginal. In two cases they were main ly central.

O b s t r u c t i o n . - Evidence of obs t ruc t ion was pre- sent in 8 of the 11 cases (Table 2b).

Fig. 2 - (Right side only injected). Large glands are present in the inguinal and iliac areas and small giands in the aortic area. The small glands may well be consequent on ob- literation of the primary glands with a subsequent hyper- trophy of smaller potential collateral nodules which will enlarge and compensate for the loss of the original para-aorfic chain. Note minimal ill-defined filling defects in the gland overlying the distal SI joint on the (R).

Fig. 3 - There is marked disparity in the appearance of the lymph glands. Those of the aortic chain show extensive replacement. In the iliac and inguinal regions, however, there is less severe infiltration in enlarged glands. It is in cases with this pattern that lymphatic blockage is likely to occur. Stasis is well shown in left iliac region.

Gradient o f Abnorma l i t y . - Glandular enlarge- men t was more obvious than glandular replacement in cases 2, 6 and 10. Replacement was more obvious than glandular en largement in cases 1, 3, 4, 8, 9 and 11 (Fig. 1, 3, 4). When the more obvious abnormal i ty was considered in any single case, a gradient of abnormal i ty became evident. There was a more severe involvement in the upper para-aortic chain extending to a relatively less marked involvement in the iliac region. A subjective assessment of this gradient is charted in Table 2b. In three cases, there was a well-marked gradient. Seven cases presented less dramatic bu t nevertheless clear-cut gradients. In two pat ients (nos. 5 and 7) the gradient was less obvious.

T H E L Y M P H O G R A M IN A B D O M I N A L T U B E R C U L O S I S 657

Fig. 4 - (Inferior venocavogram after lymphography.) The lymphogram in Fig. 1 may well be the end result of the process which is occurring here. The para-aortic glands are largely lost, only a very faint uptake is visible indicating replacement of nodes. Collateral nodules and collateral lymph channels are becoming hypertrophied. The inferior venocavogram shows obstruction from thrombosis with collateral flow occurring via the venous plexuses of the spinal canal and cord and is indicative of severe upper abdominal pathology, presumably lymphadenopathy.

DISCUSSION

A wide range of appearances have been reported concerning the lymphographic appearances of the retroperitoneal nodes in abdominal tuberculosis.

Rfittimann (1965) and Schaffer et al_ (1963) reported inflammatory patterns in the uptake of the contrast. Viamonte et al. (1963) and Bussat et aL (1966) saw marginal Idling defects while Betouliers et al. (1968), Gregl and Kienle (1969) and Johnson etal. (1971) saw central filling defects. Albrecht et aL (1967) saw both central and marginal defects. Most workers reported glandular enlargement. Suramo (1974) has studied the lymphograms on a series of patients with tuberculosis. He defined and attempted to systematise the many different changes seen within lymph nodes. Albrecht et al. (1967) reviewing retroperitoneal lymphograms in cases of tuberculosis and sarcoid, noted abnormalities predominantly in the para-aortic zones. We.have also observed this and we believe there is a definite pattern of involvement

Fig. 5 - The predominant feature is a more uniform pattern of glandular enlargement and clear-cut filling defects. There are sites of lymphovascular blockage (left iliac region), but the lymph drainage is well maintained via collaterals. Such a patient, with good drainage and little uptake of contrast material, is particularly prone to massive oil embolism. The patient did have radiological evidence of oil embolism from a lymphovenous shunt.

Fig. 6 Lymph node hyperplasia is more predominant here than filling defects. These defects are mostly ill defined. There is a suggestion of relatively further advanced infil- tration in the upper aortic nodes on the left. This may be an early indication of the more advanced pathology in the aortic area which we commonly found in our cases. However, the overall general picture resembles that of Hodgkin's disease.

within the entire retroperitoneal and iliac chain in cases of abdominal tuberculosis.

Pathophys io logy o f L y m p h a t i c Invo lvemen t in A b d o m i n a l Tuberculosis. - Small tubercles involve the lymphatics passing from tuberculous foci in the small intestine. These tubercles can extend further along the course of the mesenteric lymphatics and finally to the lymphographically visible para-aortic lymphatics. Draining lymph nodes become infected, the node enlarges and caseation produces filling defects.

Obstruction of the diseased lymphatic vessels gradually supervenes. The lymphatics become disten- ded and tortuous. When lymphatic obstruction is

658 CLINICAL RADIOLOGY

complete, the anastomotic channels enlarge and considerable varicosity can result.

Correlation o f Pathology and Radiological Findings. - T h e gland draining a tuberculous lesion may initially show hyperplasia as the gland becomes enlarged (Fig. 6). Filling defects appear. At first, they are ill-defined (Fig. 2, 6), but as the disease progresses they become more clearly delineated. The filling defects enlarge and ul t imately extend to replace the entire gland (Fig. 5). Histologically, the gland has been replaced by caseous material. The collateral channels can develop during the slow progressive obliteration of function of the pr imary glands (Fig. 4). Lymphovascular obstruction can supervene (Fig. 4 ,3 ) .

The aortic nodes seem to be the predominant site of retroperitoneal involvement. More severe involve- ment in the upper para-aortic chain as compared with that below in the iliac region suggests earliest involve- ment proximally and implies retrograde spread of the tuberculosis process along the upper para-aortic chain. This 'gradient ' is l ikely to be an outcome of the pattern of the lymphatic drainage from the intestine or from anastomoses between the various retroperitoneal groups. We have shown this gradient to apply to both glandular enlargement and glandular replacement (Table 2). The 'gradient of abnormali ty ' simply reflects the pathological effect of the disease process which is most severe at the pr imary drainage site.

D i f f e r e n t i a l Diagnosis. - Lymphographic ab- normalities in each individual gland in these tuber- culosis cases were indistinguishable from appearances in metastatic disease, the lymphomas and non-specific reactive hyperplasia.

Acknowledgements. - Our thanks goes to those members of the Department of Radiology, University College Hospital, Ibadan, Nigeria, without whose, assistance this study could not have been completed, and to the Medical Illustration Unit who produced the photographs.

We are particularly grateful to Professor S. P. Bohrer for his continuing encouragement and support.

REFERENCES

Albrecht, A., Taenzer, V. & Nickling, H. (1967). Lympho- graphische Befunde bei Sarkoidose und Lymphknoten- tuberkulose. Fortschritte auf d. Geb. der Roent- genstrahlen und der Nuklearmedizin.

Betouliers, P., Lamarque, J. L., Ginestie, J. T_, & Combes, C. (1968). Etude des aspects lymphographiques de la tuber- culose ganglionnaire. Journal de Radiologie, 49, (In.) (1) 1-6.

Bussat, P. L_, Beboux, J. M., Petite, J. & Wettstein, P. (1966). Lymphography in a patient with non-reactive tubercu- losis. American Journal of Roentgenology, 98, 436-439.

Gregl, A. & Kienle, J. (1969). Axillary lymph node tuber- culosis presenting lymphographic signs of metastasis from ipsilate~al breast cancer. Radiology, 93, 1107-1108.

Johnson, J. C., Dunbar, J. D. & Klainer, A. S. (1971)_ The pseudotumour of retroperitoneal tuberculous lympha- denitis. American Journal of Roentgenology, Radium Therapy and Nuclear Medicine, III, 554-561.

RiJttimann, A. (1965). In Lehrbuch der Roentgendiagnostik, ed. Schinz, H. R, et aL, 5, 677-699. Stuttgart Thieme.

Schaffer, B., Koehler, P. R., Daniel, C. R., Wohl, G. T., Rivera, E., Meyers, W. A. Skelley, J. F., Jr., (1963). A critical evaluation of Lymphangiography. Radiology, 80, 917-930.

Suramo, I. (1974), Lymphography in tuberculosis. Acta radiologica, Suppl. 339, 58 pp.

Viamonte, M., Jr. Altman, D., Parks, R., Blum, E., Bevilacqua, M. & Recher, L. (1963). Radiographic- pathologic correlation in interpretation of Lymphangio- adenograms. Radiology. 80, 903-916.

Wiljasolo, S. (1969). LymphographlC polymorphism in Hodg- kin's disease. Acta radiologica, Suppl 289, 89 pp.