BY DR MAIMUNA ABDULKARIM HALLIRU

DEPT OF RADIOLOGY

AMINU KANO TEACHING HOSPITAL, KANO

15/10/2014

DISCUSS THE IMAGING FEATURES OF SMALL BOWEL LYMPHOMA

OUTLINE INTRODUCTION

PATHOGENESIS

DISTRIBUTION

RISK FACTORS

CLINICAL FEATURES

HISTOPATHOLOGY

ROLE OF RADIOLOGY IN MANAGEMENT

IMAGING MODALITIES

IMAGING FEATURES

RADIOLOGY OF COMPLICATIONS

SUMMARY/CONCLUSION

INTRODUCTION

The small bowel is the longest part of the GI tract

spanning a length of about 6 metres and the mucosa of the small bowel accounts for over 90 percent of the surface of the gastrointestinal (GI) tract.

It is made up of three parts: proximally the

duodenum, jejunum and most distally, the ileum.

The small bowel has a calibre of about 3-5 cm.

Circular, circumferential mucosal folds- the plicae circulares are found most numerously in the jejunum and least in the ileum.

The small bowel has clumps of submucosal lymphoid tissue called the Peyer’s patches in the jejunum and ileum. However they are most numerous in the ileum.

(1)Buckley.J.A,Fishman.E.K; CT Evaluation of small bowel neoplasms-Spectrum of disease.RSNA 1998:18;379-392

PATHOGENESIS The small bowel is a rare site of tumours in general

and accounts for less than 2-5 percent of all GI neoplasms and 1 percent of GI carcinomas(1).

Explanations:

a) the liquid contents of the small bowel may cause less mucosal irritation than the more solid contents of the colon;

b) The relatively rapid transit of intestinal contents through the small bowel may provide shorter exposure of its mucosa to carcinogens;

c) The much lower bacterial load in the small bowel may result in decreased; conversion of bile acids into potential carcinogens by anaerobic microorganisms

d) Benz(o)pyrene, a known carcinogen present in various foods, is converted in less toxic metabolites by benz(o)pyrene hydroxylase, which is present in much higher concentrations in the small intestine compared to the stomach and colon;

e) The increased lymphoid tissue with a high level of (secretory) IgA expression in the small bowel may be protective

Survival from primary malignancies of the small intestine has not improved in parallel with significant advances in diagnostic imaging over the last four decades.

Curative treatment depends on early diagnosis and surgical resection.

(2)Maceneaney P.M, Gasparaitis A.E;Diagnosis of Small-Bowel Tumors pp359;1-14

Unfortunately,many cancers of the small bowel are diagnosed at an advanced stage, after the window of opportunity afforded by local disease has elapsed.

Maglinte and colleagues(2) showed that there was an average delay of almost 9 months between onset of symptoms and diagnosis.

Several factors contributed to this delay:

-delayed ordering of appropriate investigations by the clinician.

-misinterpretation of investigations by radiologists.

DISTRIBUTION

Small bowel lymphoma accounts for about 20% of all small bowel tumours.

The jejunum and ileum are almost equally affected. The distal ileum is the most common site, owing to the large amount of lymphoid tissue that is present here.

Most GI lymphomas occur in middle-aged people.

Burkitt’s lymphoma is commoner in children.

Enteropathy associated T-cell lymphoma is commoner above 60 years of age.

Males and females are equally affected.

The ileocecal region is the most common location for primary small bowel lymphoma (children and young adults), whereas lymphoma is more often found in the proximal jejunum in patients with celiac disease.

Multicentric lymphoma involving different segments of the gastrointestinal tract occurs in 10% to 50% of cases.

Non-Hodgkin's lymphoma is the commonest variety that involves the GI tract.

Almost 90 percent of primary NHLs of the small bowel are of the B-cell type.

Usually intermediate or high grade with large cell features.

Apart from cases related to celiac disease, T-cell lymphomas are rare, as are Burkitt’s lymphoma and Hodgkin’s disease of the small bowel.

Burkitt’s lymphoma of the bowel is usually confined to the ileocecal region.

RISK FACTORS

Celiac disease.

Crohn's disease.

Systemic Lupus Erythematosus.

Immunocompromised state.

A history of chemotherapy.

CLINICAL FEATURES

The commonest clinical features associated with small bowel lymphoma are abdominal pain, fatigue, malaise,gastrointestinal bleeding, nausea and vomiting, and weight loss.

Palpable mass in 33%

Obstructive features and perforation occur relatively late; in about 25% .

CLINICAL FEATURES

These nonspecific clinical features, coupled with the low incidence of small-bowel tumours, result in a low index of suspicion on the part of the physician and the radiologist and contribute to the slow diagnosis of such tumours.

The criteria for establishing the diagnosis of primary gastrointestinal lymphoma are:

a) Absence of palpable lymphadenopathy;

b) Normal peripheral blood smear and bone marrow biopsy.

c) Absence of mediastinal lymphadenopathy on chest x-ray.

d) Disease grossly confined to the affected small bowel segment, as confirmed by diagnostic imaging, endoscopy or laparotomy.

e) Regional lymphadenopathy ;and,

f) Absence of hepatic or splenic tumour involvement except via direct extension from primary bowel involvement.

Histopathologic types of lymphoma that

may involve the small intestine include:

malignant lymphoma (in celiac disease).

B-cell lymphoma.

Immunoproliferative small intestinal disease (Mediterranean lymphoma).

HISTOPATHOLOGY & STAGING

Low grade B-cell lymphoma (lymphoma of mucosa associated lymphoid tissue).

Follicular lymphoma.

Burkitt's lymphoma (in children).

Mantle cell lymphoma.

Rarely, Hodgkin’s disease.

STAGING

Classification: Ann Arbor (classic), Musshoff

(modified Ann Arbor) and Blackledge (1990).

Recently, these classifications system have been

superseded by a Revised European-American

Lymphoma (REAL) classification, which includes

entities such as T-cell lymphoma, maltoma and

mantle-cell lymphoma.

Ann Arbor Classification:

I E: Single GI tumour confined to small intestine without lymph nodes.

II E: GI tumour focus + Regional Lymph node involvement on one side of the diaphragm.

III E: GI tumour focus + non-resectable Lymph nodes on both sides of the diaphragm.

III ES: III + splenic involvement.

IV E: GI tumour focus+ disseminated involvement of extra-lymphatic systems (i.e bone marrow, liver).

PATTERNS OF SMALL BOWEL LYMPHOMA

Circumferential infiltration of a small bowel segment:

§ Results in a variable length of thickening and effacement of folds.

§ Widening of the lumen rather than narrowing from infiltration of muscularis layer with destruction of the myenteric plexus leading to aneurysmal dilatation, often at the antimesenteric segment. A.k.a Intestinal aneurysm.

Nodular and polypoid lesions can be variable in size and irregularly distributed.

These are sometimes reported to cause intussusception. This is a relatively rare manifestation of small-bowel lymphoma and may represent disease originating in mantle cells or mucosa-associated lymphoid tissue (MALT).

Mucosal wall thickening with narrowing,

stricturing and occassionally shouldering may be

seen.

Endoexoenteric lesions that can cause fistulas

ROLE OF RADIOLOGY IN MANAGEMENT

In making a diagnosis.

In staging.

In assessing complications of the disease.

IMAGING MODALITIES

Plain Radiograph

Abdominal ultrasound scan

Contrast Radiographic studies

Abdominal Computed Tomography scan

Magnetic Resonance Imaging

Nuclear Imaging

Angiography

PLAIN ABDOMINAL X-RAY

Small bowel x-rays are currently the most widely used studies for investigation of focal small intestinal lesions.

Plain abdominal radiographs may reveal obstruction, a calcified mass or evidence of hollow viscus perforation, but their overall yield in uncomplicated small bowel tumours is very low.

ULTRASONOGRAPHY

Endoscopic ultrasonography or endoscopic ultrasound (EUS) has been the most recent addition to the armamentarium of diagnostic modalities for the examination of the small bowel.

This new technological achievement not only provides high resolution imaging of the gastrointestinal wall and surrounding structures, but also allows interventional diagnostic and therapeutic procedures under real-time EUS guidance.

EUS image showing 5 layers of the gastric wall. 1, 3, and 5 = first,

third, and fifth layers are hyperechoic (white); 2 and 4 = second

and fourth layers are hypoechoic (black). Transducer (tr) is

surrounded by a water-filled balloon (arrows).

Mixed hypoechoic gastric tumour (T) disrupting the normal 5-layer

architecture at this point (long arrow). Tumour extends into the

hypoechoic muscularis propria layer (black arrows). The

hyperechoic serosal layer (short arrows) is intact.

ULTRASONOGRAPHY

However, the ability of EUS in detecting and staging small bowel lesions appears to be most applicable only to ampullary tumours, carcinoid tumours and vascular lesions.

Thus the transabdominal route is still the conventional mode employed in the general sonographic assessment of small bowel lymphoma.

The diagnostic yield of this procedure is low. This

is due to the presence of luminal gas within the

bowel.

Sonogram of the left upper quadrant of abdomen showing dilated and thickened small bowel loop (black arrow) with luminal narrowing (red arrow).

Large mesenteric lymph nodes in a case of small bowel lymphoma.

CONTRAST RADIOGRAPHIC STUDIES

Detailed barium evaluation of the small bowel is

difficult due to the presence of multiple peristaltic

intestinal loops overlapped in a limited area.

This results in lower sensitivity and specificity of

barium studies in the small bowel, compared to the

equivalent study of the stomach and colon.

The reported sensitivity of the conventional (non-

enteroclysis) small-bowel study (SBS) varies

widely.

An abnormality demonstrated by SBS was present in up to 83 percent of cases of primary small-bowel malignancies, but the tumour was directly visualized in less than 50 percent of cases(2).

This suboptimal diagnostic performance of the conventional barium SBS inevitably leads to false-negative results and diagnostic delays.

Enteroclysis is the preferred method for detecting small, resectable small bowel tumours.

(2) Maceneaney P.M, Gasparaitis A.E; Cancer of the Upper Gastrointestinal Tract; Ch. 20-Diagnosis of Small-Bowel Tumors pp359

The routine small bowel follow through (SBFT) is simple, inexpensive and non-invasive, but is relatively insensitive.

Much more accurate information can be obtained using enteroclysis. In this double contrast X-ray study, the descending duodenum is first intubated.

Smooth muscle relaxants such as hyoscine and glucagon are used to dilate the small bowel.

Barium and methylcellulose are then infused under pressure into the small intestine.

This method produces distension of the bowel and allows the fluoroscopist to follow the movement of the contrast material through the gut.

As compared to the traditional small bowel series, enteroclysis permits better visualization not only of the intestinal lumen but also of the mucosal surface.

(3)D. Xynopoulos, A.A. Mihas, E. Paraskevas, D. Dimitroulopoulos, D.M. Heuman, A.A. Mihas. Small bowel tumours. Annals of Gastroenterology 2002;15(1):18-35.

Transient delay in passage of contrast can identify areas of partial obstruction that are otherwise extremely difficult to locate.

In one series, enteroclysis had a sensitivity of 90% for small bowel tumours, versus only 33% with SBFT(3).

The small-bowel enema shows an ileal segment with thickened folds. At the antimesenteric border a short outpouching (arrows) is visible.

The small bowel enteroclysis image shows thickened mucosa with nodular appearance and dilatation of the lumen.

Enteroclysis study demonstrating enteric contrast material filling a large cavity in a small-bowel lymphoma.

Small-bowel series depict aneurysmal dilatation of a segment of ileum

Short segment (left lowermost loop) with diffuse thickening of the valvulae

conniventes and a subtle background nodular pattern consistent with “maltoma.”

ABDOMINAL CT SCAN

Computed tomography has been employed in the assessment of small-bowel pathology in two settings:

(1) in patients with bowel obstruction and in whom barium studies are unpleasant, difficult, and risky.

(2) when staging tumours. Computed tomography evaluates the level, grade, and (frequently) the cause of the obstruction.

In patients with intestinal obstruction secondary to a small bowel tumour, the tumour is relatively large and may therefore be identified by CT.

However, diagnosis of early non-obstructive tumours of the small bowel by standard CT is usually serendipitous.

Neoplastic disease should be suspected on CT if the thickness of the wall of the small bowel is > 1.5 cm or if there are discreet mesenteric masses larger than 1.5 cm.

Radiologically, diagnosis and staging are performed with a combination of CT and barium studies.

Computed tomography may also be used to guide percutaneous biopsy of the bowel or a nodal mass.

Computed tomography (CT) can identify masses but is insensitive for diagnosis of small tumours and has a limited ability to differentiate between tumour types.

Large adenocarcinomas and lymphomas are often mistaken for each other.

Its greatest utility seems to be in the preoperative staging and evaluation of metastases.

(3)D. Xynopoulos, A.A. Mihas, E. Paraskevas, D. Dimitroulopoulos, D.M. Heuman, A.A. Mihas. Small bowel tumours. Annals of Gastroenterology 2002;15(1):18-35.

Computerized tomographic (CT) enteroclysis, a combination of CT scan with barium infusion through a nasogastric (NG) tube, has been the subject of recent favourable reports from Europe but remains an investigational tool at present (3).

The images acquired overcome the problem of overlapping bowel loops encountered in conventional barium studies, and there is the potential of performing multiplanar reformatting.

Computed tomography tends to be very sensitive but not specific for the detection of mesenteric infiltration, regional lymphadenopathy, and distant metastases(2).

(2) Maceneaney P.M, Gasparaitis A.E; Cancer of the Upper Gastrointestinal Tract; Ch. 20-Diagnosis of Small-Bowel Tumors pp359

CT scan demonstrates a polypoid mass (arrow)

CT scan demonstrates a bulky mass encasing the small bowel just beyond the ligament of Treitz (arrow). In addition to the wall thickening, the marked luminal dilatation (aneurysmal dilatation) helped differentiate this lymphoma from adenocarcinoma.

CT scan demonstrates infiltration of the ileum in the left lower quadrant (arrow). The mass is exophytic and partially necrotic.

CT scan of the abdomen shows a loop of small bowel in the mid-abdomen with a markedly thickened wall.

Dilated lumen at the site of the mass and prestenotic dilatation of the duodenum (red arrow).

Lymphoma in the terminal ileum.

A huge endoexoenteric mass involving a loop of ileum extending intoadjacent tissues with mural gas bubbles extending into adjacent tissues

indicating an enteric fistula.

Huge multilobullated abdominal mass in a patient with small bowellymphoma due to lymphadenopathy.

MAGNETIC RESONANCE IMAGING Magnetic resonance imaging (MRI) is used for

staging cancers and not for the primary detection of small bowel tumours.

Development of contrast agents, coils, and rapid pulse sequences have improved MRI of the GI tract.

Fast pulse sequences allow for imaging during a breath-hold and minimize the motion artefact associated with peristalsis and respiration.

Magnetic resonance (MR) has been used to evaluate small-bowel obstruction, and MR enteroclysis has been reported.

Bowel contrast is important in MR to avoid mistaking bowel loops for adenopathy or mesenteric masses.

Positive-contrast agents such as gadolinium, manganese, or ferric ammonium citrate reduce T1 relaxation times.

These agents can accentuate “ghosting” artefacts from peristalsis. Rapid imaging techniques and anti-peristaltic agents minimize these effects.

Negative contrast agents may be classed as diamagnetic preparations (e.g., barium) and superparamagnetic iron oxides.

These negative agents represent the major options for radiologists.

As more contrast preparations are developed and approved, it is likely that oral contrast administration will become routine and that the role of MRI in small-bowel pathology will evolve.

Small bowel lymphoma typically shows as asymmetrical but circumferential wall thickening with associated luminal dilatation (intestinal aneurysm).

Significant enlargement of mesenteric lymph nodes.

Low signal intensity on T1, slightly increased on T2, hypovascular and thus very little contrast enhancement.

Diffuse mural thickening in a loop of small bowel due to lymphoma.

Thickening in a loop of small bowel due to lymphoma.

Lymphoma in the proximal small bowel seen as circumferential wall thickening (arrow).

Ileal wall thickening due to B-cell lymphoma

Ileal lymphoma with mesenteric lymphadenopathy.

Mesenteric lymphadenopathy (red arrows).

NUCLEAR IMAGING Small bowel lymphoma typically are depicted as

hot spots due to increased uptake of radionuclide.

PET-CT the usual modality of investigation.

Diffuse large B-cell lymphoma

Lymphoma in proximal jejunum.

EATL lymphoma in a patient with celiac disease.

B-cell Lymphoma in proximal small bowel.

ANGIOGRAPHY (DSA, MRA, CTA) Angiography may be used to evaluate and

embolize bleeding from ulcerated and vascular, more aggressive subtypes.

Angiography is occasionally used as an aid

to surgical planning.

ANGIOGRAPHY (DSA, MRA, CTA) Lymphoma is a relatively hypovascular tumour.

Therefore findings on angiography are usually:

i- Mild tumour blush.

ii- Splaying/Displacement of the mesenteric vessels.

iii-Rarely, extravasation of contrast medium in aggressive, bleeding lesions.

Superior mesenteric angiogram showing extravasation of contrast fromthe sixth jejunal branch (arrow).

Enteropathy associated T-cell lymphoma.

Pre- embolization. Post- embolization.

RADIOLOGY OF COMPLICATIONS

INTUSSUSCEPTION

This complication is often encountered with the polypoid or nodular form of lymphoma where the tumour acts as a lead point.

Characteristic reniform appearance of ileocolic intussusception inthe right iliac fossa. Proximal small bowel dilatation.

Ileal-ileal intussusception in a patient with multifocal small bowel lymphoma .

MESENTERIC LYMPHOMA Multiple homogeneous masses encasing the

mesenteric vessels “sandwich sign”.

Large “cakelike,” mass with low-attenuation areas of necrosis displacing small bowel loops.

Ill-defined infiltration of mesenteric fat, particularly after successful chemotherapy.

Bulky retroperitoneal adenopathy.

Small bowel and mesenteric lymphoma

Sandwich Sign of Mesenteric Lymphoma. A mesenteric artery (arrow) is sandwiched between two homogeneous isodense masses of lymphoma.

Sandwich Sign of Mesenteric Lymphoma. A mesenteric artery (arrow) is sandwiched between two homogeneous hypoechoic masses of lymphoma ; l.

ENTERIC FISTULAE/PERFORATION Seen with the endoexoenteric /exophytic forms

which are associated with necrosis, extension into adjacent tissues eventually leading to fistulae and bowel perforation.

DIFFERENTIAL DIAGNOSIS

Tuberculosis

Inflammatory small bowel disease

Carcinoma.

TUBERCULOSIS

Contrast enhanced CT shows gross circumferential wall thickening of the jejunum in a patient with gastrointestinal dissmeninated mycobacterium avium intracellulare.

INFLAMMATORY BOWEL DISEASE

Crohn’s disease of the small bowel with mucosal wall thickening (black arrows) and fat stranding (white arrows).

INFLAMMATORY BOWEL DISEASE

Thick walled mass in terminal ileum, representing small bowel.

ADENOCARCINOMAAn irregular mass in the proximal jejunum (upper image).

There is a large conglomerate of hypodense lymph nodes in the adjacent mesentery, consistent with necrotic lymph node metastases (lower image).

ADENOCARCINOMA

Extensive wall thickening of the proximal jejunum with aneurysmatic dilatation (arrow).

TREATMENT AND PROGNOSIS

Malignant lymphoma of the small bowel is treated with surgical resection, usually followed by chemotherapy to prevent perforation.

Radiation therapy may also be used.

Poor prognosis is associated with:

§ Stage greater than IIE (nodal disease above and below the diaphragm).

§ Tumour size greater than 10 cm

§ T cell type

§ Presentation as an acute abdomen

SUMMARY/CONCLUSION Small bowel lymphoma is rare and due to low

index of suspicion on the part of both clinicians and radiologists, there is usually delay in diagnosis and treatment with resultant poor prognosis.

Be conversant with clinical presentation and imaging findings to redirect physicians where necessary and to increase diagnostic accuracy.

THANK YOU FOR YOUR TIME AND ATTENTION