CT features of peripheral T-cell lymphoma in the gastrointestinal tract in Chinese population and...

RADIOLOGY—ORIGINAL ARTICLE jmiro_2329 143..150

CT features of peripheral T-cell lymphoma in thegastrointestinal tract in Chinese population andliterature reviewLing Zhu, Guangyao Wu, Prasanna Ghimire and Liying Xu

Department of Magnetic Resonance Imaging, Zhongnan Hospital of Wuhan University, Wuhan, Hubei Province, China

L Zhu MBBS, MD; G Wu MD, PhD; P GhimireMBBS, MD; L Xu MD, PhD.

CorrespondenceProfessor Guangyao Wu, Department of

Magnetic Resonance Imaging, Zhongnan

Hospital of Wuhan University, 169 East Lake

Road, Wuhan 430071, Hubei Province, China.

Email address: [email protected]

Conflict of interest: None.

Submitted 2 April 2011; accepted 18 May

2011.

doi:10.1111/j.1754-9485.2011.02329.x

Abstract

Introduction: The aim of the study was to retrospectively investigate the CTfeatures in peripheral T-cell lymphoma (PTCL) of the gastrointestinal tract inthe Chinese population.Methods: Computed tomography scans of 15 histopathologically proven casesof PTCL involving the gastrointestinal tract were retrospectively reviewed forcharacteristics such as sites, multiplicity, morphological features, the patternand degree of contrast enhancement, lymphadenopathy, involvement of otherorgans and complications such as perforation, intussusceptions, ascites andso on. By reviewing the literature, CT findings of PTCL involving the gas-trointestinal tract were compared with that involved by B-cell lymphoma.Results: PTCLs involved the stomach and intestine in six and nine patients,respectively. Multiplicity was seen in seven patients, and solitary involvementwas seen in eight. At CT, wall thickening was the predominant finding in allcases with an exception of one intestinal PTCL case presented as polypoidmass. Among the 14 patients, the gastric or bowel wall thickening was mild(<10 mm) in three, moderate (10–20 mm) in 10 and severe (>20 mm) in one.Nine cases demonstrated mild homogeneous enhancement, whereas sixshowed mild heterogeneous enhancement. Lymphadenopathy was present ineight patients, five of which were non-bulky (diameter <5 cm) and diffusetype and the rest (three) were non-bulky and localised type. Other organswere involved in four patients. Perforation as complication was evident in onegastric and five intestinal lymphomas (55.6%). Among the nine intestinalPTCLs, seven of the patients were male (77.9%) and the rest (two) werefemale with a median age of 37.1 years old. Intestinal PTCLs predominantlyinvolved colon (n = 5). Other sites of involvement were ileum (n = 1), ileo-caecum (n = 1), ileum and ileocaecum (n = 1) and entire bowel segment fromdistal ileum to transverse colon (n = 1).Conclusion: PTCLs have some distinguishing radiological features from B-celltype gastrointestinal lymphomas as mild or moderate gastric or bowel wallthickening and higher incidence of perforation with multiplicity. In China,intestinal PTCLs are not usually associated with coeliac disease and commonlypresent in a young male population with colon being the most frequent site ofinvolvement.

Key words: coeliac disease; computed tomography; diffuse large B-cell lym-phoma; gastrointestinal tract; peripheral T-cell lymphoma.

Introduction

Primary gastrointestinal (GI) lymphoma is very rare,constituting 1–4% of all malignancies that affect the GI

tract. Stomach is the most common site to be involved(>50%) in GI lymphoma followed by small bowel (20–50%) and colon (4–6%).1 The majority of primary GIlymphomas are non-Hodgkin lymphoma of B-cell

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Journal of Medical Imaging and Radiation Oncology 56 (2012) 143–150

© 2012 The AuthorsJournal of Medical Imaging and Radiation Oncology © 2012 The Royal Australian and New Zealand College of Radiologists 143

lineage.2 T-cell types are relatively rare making up 4–6%of all GI lymphomas, and the incidence varies in differentregions and races.3 Common sites of involvement byperipheral T-cell lymphomas (PTCLs) in the order ofoccurrence are the bone marrow followed by skin, lungand liver with the GI tract involved in less than 10%.4

The clinical process of GI PTCLs is more aggressive thanB-cell type. The treatment is not very effective and theprognosis is extremely poor with 5-year survival rate ofonly 10–45%.5 Computed tomography can evaluate theinvolvement and provide information on staging as wellas assessing treatment response in GI lymphomas. Themajority of GI tract CT literatures dealt on B-cell lym-phomas with relatively few on PTCLs. In this article, wediscuss the CT features of GI PTCLs in the Chinesepopulation and briefly review the existing literature.

Methods

Patients

A retrospective review of the pathological database fromJanuary 2004 to October 2010 showed 19 patients diag-nosed with PTCLs involving GI tract. Among thesepatients, 17 had performed CT scan at our institutions.We excluded two cases that had received chemotherapyprior to undergoing CT scan. Among the 15 patients, 10of the patients were male and five were female with amedian age of 35.4 years (range 19–59 years). Thecomplaints of patients were abdominal pain in 12 ofwhich six had concurrent fever. Abdominal distensionwas present in two cases, while fever was the onlycomplaint in one patient. Four patients had cervical andtwo patients had inguinal lymphadenopathy. One patienthad history of being operated for ulcerative colitis. Theaverage duration from the development of symptomsto the time of CT examination ranged from 1 day to9 months. Being a retrospective study, no any approvalfrom the review board or patient consent was requiredbased on the hospital guidelines.

Image acquisition

Computed tomography scan was performed using a16-slice spiral CT scanner (Siemens Somatom Sensation16, Siemens AG, Forchheim, Germany) in 14 of them,while one was examined on a single slice spiral CTscanner (Piker PQ 6000, Picker International Inc., Cleve-land, OH, USA) using 8-mm collimation and a pitch of 1.5from the dome of diaphragm to the level of pubic sym-physis. Patients were kept fasting overnight. Patientswho were to have bowel scanned were advised oralmagnesium sulphate solution in the evening prior to theday of examination. Patient had orally taken 800 mL ofwater as negative contrast medium 1 h before and justprior to the examination. One patient had received1000 mL of a 3% diluted diatrizoate meglumine and

diatrizoate sodium solution (Gastrografin, Shanghai SinePharmaceutical Co. Ltd., Shanghai, China) as a positivecontrast. An antispasmodic (20 mg of anisodamine – aMuscuranic-receptor blocker extracted from a Chineseherb) was given intramuscularly 10 min prior to exami-nation. Patients were given 1.5 mL/kg of an intravenousbolus of non-ionic contrast medium Iopromide (Ultravist300, Bayer Schering Pharma, Berlin, Germany) at a rateof 3 mL/s via an 18-gauge intravenous catheter placed inthe antecubital vein connected to a power injector.Contrast-enhanced scans were obtained at 30 and 70 sfollowing intravenous injection of the contrast agent.

Image review

Computed tomography scans were reviewed indepen-dently by two radiologists who had more than 10 yearsof experience in GI radiology. The reading radiologistswere blinded to the clinical, radiological as well as finalpathological diagnosis. The CT images were analysedand noted for the following parameters – sites ((i)stomach – gastroesophageal junction, cardia, fundus,body, antrum and pylorus; (ii) intestine – duodenum,jejunum, ileum, colon and rectum), focality (solitarywhen single lesion is present or is continuous despitemultiple site involvement and multiplicity when lesionsare multiple and discontinuous), morphological features(wall thickening was considered present when the thick-ness was more than 5 mm in stomach6 or 3 mm inintestine7 with the lumen well distended; thickening ofthe wall was labelled as either mild (<10 mm), moderate(10–20 mm) and severe (>20 mm)7 and the pattern anddegree of contrast enhancement (the pattern consideredhomogeneous or heterogeneous depending uponwhether there is less or more than 10 HU of difference inenhancement present of the affected segment; thedegree of enhancement was considered mild if less thanthat of erector spinae, moderate if less than 90 HU butmore than that of muscle, and marked enhancement ifmore than 90 HU). Lymphadenopathy was diagnosedwhen the lymph nodes’ short diameter was greater than1 cm. Lymph nodes were considered bulky if >5 cm indiameter on axial sections or were conglomerate8 andnon-bulky if lymph nodes were minimally enlarged(<5 cm in diameter) and separated. Lymphadenopathywas considered localised or diffuse depending uponwhether lymphadenopathy was regional (confined to thedrainage area of the involved segment of gut) or wide-spread (beyond the area of drainage). Concurrentinvolvement of other organs and complications (perfo-ration, intussusceptions, ascites and so on)9 were alsonoted. The CT pattern of gastric involvement was con-sidered: (i) diffuse (wall thickening >50% of the length ofthe stomach); (ii) segmental (wall thickening �50% ofthe length of the stomach); or (iii) focal involvement(forming a localised mass lesion or a polypoid form).10

The CT patterns of intestinal involvement were described

L Zhu et al.

© 2012 The AuthorsJournal of Medical Imaging and Radiation Oncology © 2012 The Royal Australian and New Zealand College of Radiologists144

as either circumferential form, cavitary form, localisedpolypoid form or a mesenteric nodal form. Hepatomegalywas defined when the liver was greater than 13 cm inlongitudinal diameter at the mid-clavicular line, and sple-nomegaly when the craniocaudal measurement of thespleen was greater than 10 cm.9

Results

Pathological diagnosis

Four gastric PTCLs were diagnosed by endoscopic biop-sies and the rest (two) of the gastric cases were diag-nosed from surgical specimens. Two intestinal PTCLswere diagnosed from endoscopic biopsies, while otherseven intestinal cases were diagnosed from surgicalspecimens. Immunohistochemistry tests were per-formed, with makers CD3 (cluster of differentiation),CD5, CD43 and CD45RO being positive in all cases.

The CT appearances of GI PTCL (Table 1) andpathology

Gastric PTCL

The body and gastric antrum were involved in five caseseach. Multiplicity was observed in three patients, whilethe remaining three showed solitary involvement. All sixcases had bowel wall thickening with segmental patternpresent in three cases while a diffuse pattern was noticedin two cases (Fig. 1a–d). One case showed mild, whilefour had moderate wall thickening. Severe wall thickeningmeasuring 45 mm was seen in one case, which had comb-like mucosa. All the six cases had mild enhancement afteradministration of contrast agent with four being homo-geneous and the rest (two) being heterogeneous. Onepatient had localised non-bulky lymphadenopathy, whiletwo had diffuse non-bulky lymphadenopathy. Othersites involved included liver (n = 2), spleen (n = 2), lung(n = 1) and nasopharynx (n = 1). Perforation wasdetected in one case during the surgery.

Intestinal PTCL

The sites of involvement by intestinal PTCL included onlyileum (n = 1), ileocaecum (n = 1), ileum and ileocaecum(n = 1), intestinal segment from distal ileum to trans-verse colon (n = 1) and only colon (n = 5). One case wasof polypoid pattern. Eight cases were of circumferentialpattern with the thickness of the bowel wall being mildin two and moderate in six cases. One case presentedas an ‘aneurysmal dilatation’ (Fig. 2a–d). All nine casesdemonstrated mild enhancement, five of which werehomogeneous and the rest (four) were heterogeneous.Lymphadenopathy was seen in three cases as a diffuseand non-bulky type, while two were localised and non-bulky type. One case had liver involvement. Perforationwas present in five cases (Fig. 3a–d). Ta

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CT features of GI PTCL


Fig. 1. Computed tomography scans

obtained in a patient with peripheral T-cell

lymphoma involving the entire stomach. (a)

Axial plain CT demonstrates thickening with

irregular inner wall. (b) Contrast-enhanced CT

scan in arterial phase shows mild heteroge-

neous enhancement of the thickened wall

(white arrow). (c) Multiple planar reconstruc-

tion contrast-enhanced CT shows diffuse

severe thickening of the entire wall of

stomach with the hypertrophied mucosal

folds appearing comb-like (white arrow). (d)

High-power photomicrograph (original mag-

nification, ¥400; immunostain CD3 (cluster

of differentiation) shows pleomorphic T-cell

positive for CD3.

a b

c d

Fig. 2. Peripheral T-cell lymphoma of the ter-

minal ileum in a patient who presented with

abdominal pain. (a) Axial plain CT shows the

wall of distal ileum having circumferential

moderate thickening with ulceration with

‘aneurysmal dilatation’ (white arrow). Axial

(b) and multiple planar reconstruction (c)

contrast-enhanced CT in arterial phase show

mild, heterogeneous enhancement (white

arrow). (d) High-power photomicrograph

(original magnification, ¥400; haematoxylin-

eosin stain) shows very large pleomorphic

cells, lots of mitotic figures, prominent nuclei

and Reed–Sternberg-like cell (black arrow).

a b

c d

L Zhu et al.


Discussion

Epidemiology, clinical and pathologicalcharacteristics of intestinal PTCLs

GI PTCLs, which were previously called malignant histio-cytosis, originate from T-cell of the GI tract mucosa.PTCL is diagnosed when tumour cells variably expressthe mature T-cell antigens CD2, CD3, CD4, CD5 and CD7on immunohistochemical staining and T-cell receptor bchain rearrangement.11 Earlier, intestinal PTCLs wereconsidered to have association with CD and were namedenteropathy-associated T-cell lymphoma (EATL). It isvery rare in most parts of the world but has beenobserved with increasing frequency in areas where thereis a high prevalence of CD, particularly in NorthernEurope. Recent studies show that all EATLs are notassociated with CD.12 According to the new World HealthOrganization classification system, there are two typesof EATL: type 1 is associated with CD and accounts forthe majority of cases in Western countries, whereas type2 is not associated with CD. The criteria for EATL includepresence of (i) intestinal T-cell lymphoma; (ii) histologi-cal indicators of enteropathy (intraepithelial T lympho-cytosis �40 lymphocytes per 100 epithelial cells); and(iii) a cytotoxic phenotype of CD4-CD8+ or CD4-CD8-.13

The majority of PTCLs in Western countries are EATLs,which occur mainly in middle-aged and elderly people(56–60.1 years) with no gender predilection. About 49%

of these patients have a history of CD. EATL has a poorprognosis with a mortality rate of 84.0% and an overallmedian survival time of 4 months. The EATL patientsoften complain of abdominal pain, weight loss or presentwith intestinal obstruction. CD is rare in Far East Asia14

and only a few cases have been reported in China, Koreaand Japan.15–17 Unlike jejunum that is the most preferredsite of involvement in the Western population, studiesdone in Chinese population have shown that intestinalPTCLs are more common in colon, followed by smallbowel (including ileocecal region) and simultaneousinvolvement of small and large intestines.18,19 In ourgroup, colon is the most preferred site of involvement,which is similar to the existing literatures. In a study thatwas carried out in Zhejiang Province (an area in southernChina where staple food is rice rather than wheat), fourout of 64 patients with chronic diarrhoea were diagnosedwith CD, accounting for 6.5% of the patients surveyed.They speculate that CD may not be rare in China with theprevalence higher in northern regions, where wheat isthe main staple food. Studies done in China showed thatintestinal PTCL is more common in young male with feverand haemotochezia. Majority have no histological evi-dence of enteropathy, with the overall median survivaltime of 3 months. Epstein–Barr virus has been noted tohave a possible association in some studies. In ourstudy, the patients were all from southern China with amean age of 37.1 years with male predominance. Theyhad neither history of malabsorption nor histological

Fig. 3. Computed tomography scans

obtained in a patient with peripheral T-cell

lymphoma involving the terminal ileum to

transverse colon. (a) Axial plain CT shows cir-

cumferential moderate thickening of the

bowel wall (white arrow) and ascites in the

peritoneal cavity. (b) and (c) Axial contrast-

enhanced CT in arterial phase shows mild,

heterogeneous enhancement (white arrow)

with air bubbles in the space between two

small bowel loops (black arrow) as an evi-

dence of perforation. (d) High-power photo-

micrograph (original magnification, ¥400;

immunostain cluster of differentiation 45RO)

shows pleomorphic T-cell marked with the

T-cell marker cluster of differentiation 45RO.

a b

c d



evidence of CD that is similar to the existing literatures.The reason for the variation in presentation may berelated to the different pathogenesis of the disease asmentioned previously. As the occurrence of PTCLs isrelatively rare, we cannot reliably delineate the fre-quency and preferential site of involvement in the GItract. Our present study thus faces the drawback oflimited number of cases.

Distinct and similar CT characteristics of GIPTCLs and B-cell lymphomas

Although radiologically it is difficult to differentiatePTCLs involving the GI tract from other histopathologi-cal types, some features however favour towards itsdiagnosis. Stomach is the most frequent site for B-celllymphomas with distal ileum being the most commonsite in small bowel. PTCLs, however, are seen to have ageographic variation, with jejunum more common inWestern and colon in the Chinese population. Accordingto the literature, the incidence of multiplicity is higherin PTCL (50–72%), while it is only 10–25% in B-celltype.20 The percentage of multiplicity in our group is46.7%, which is slightly below the incidence reportedelsewhere. With an exception of one having polypoidpattern and another with severe wall thickening, therest (13) of the cases of PTCLs showed mild to mod-erate thickening of lumen. Although the number ofcases is limited, this study showed that PTCLs seldomhave severe bowel wall thickening in contrast to B-celllymphomas. The macroscopic features of PTCLs in thesmall bowel include thickened plaques, ulcers or stric-tures, whereas most B-cell lymphomas present as exo-phytic or annular tumoural masses. Similar findingswere also observed in the colon.20 Several studies men-tioned extensive mucosal ulcerations as the most dis-tinguishing feature in colonic PTCL.21 This pathologicalfeature probably relates to the fact that PTCL usuallyoccurs in the layer of mucosa while B-cell type origi-nates from the layer of submucosa. Thus, when thelesion is confined to the mucosa with an absence of, oronly mild mural involvement, CT is not the ideal modal-ity for detecting lesions in the GI tract.9

The incidence of bowel perforation is higher in PTCLs(41–50%) than in B-cell lymphomas (<30%).20 It isseen that tumour perforation is extremely rare ingastric and colorectal lymphomas but higher in lym-phoma involving the small bowel.9 Almost half of thePTCLs and one-third of B-cell lymphomas present asperforation. In our study, perforation occurred in fivecases of colon lymphoma (55.6% of the nine intestinalPTCLs). None of these patients had history of chemo-therapy. Besides, one gastric PTCL was found to beperforated at surgery. These results differ from existingliterature.9 The prevalence of perforation in PTCLs maybe attributed to its characteristic pathological features,which include angiocentric and angioinvasive infiltration

of the vascular walls by lymphoid cells with varyingdegrees of cytological atypia, which caused vascularocclusion with subsequent development of ischemicnecrosis of both the tumour and the normal tissuesresulting in bowel perforation.11

The lesion of GI PTCLs shares some common featureswith B-cell lymphomas. Both show homogeneous isoat-tenuating or hypoattenuating bowel wall thickening atCT, rarely invading the surrounding structures. Bothvariants demonstrate similar contrast enhancementpatterns. Lymphomatous involvement of other paren-chymal organs usually results in the increase in size.Severe and diffuse lymphadenopathy can help in thedifferentiation from GI carcinoma.22 Young reported that12% of gastric lymphoma had mucosal folds hypertro-phy. The severe mucosal folds hypertrophy, whichappears as comb-like bowel wall thickening as seen inone of our cases, is one of the features of lymphoma.23

When lesions occur in small bowel and involve the auto-nomic plexus in lamina propria, it can cause decrease inmuscle tension, leading to bowel wall dilatation, thusfinally appearing as ‘aneurysmal dilatation’ in CT as inone of our cases (Fig. 2).24

Differentiation from other GI carcinomasand pathologies

Although differentiating gastric lymphoma radiologicallyfrom gastric carcinoma is not so accurate, certain fea-tures do favour towards the diagnosis of gastric lym-phoma on CT. The most important features that suggestlymphoma include relative preservation of the fat planesurrounding the gastric wall, absence of obstruction andusually no invasion of surrounding structures despite thesize of the malignancy. Besides, presence of lymphad-enopathy extending below the level of renal hilum alsofavours gastric lymphoma rather than gastric carci-noma.25 It has been seen that gastric carcinoma showsat portal venous phase higher (>20 HU) or similarenhancement to that in arterial phase. Gastric lymphomausually shows only mild enhancement with no significantdifference in two phases (<20 HU).26 Carcinoma is morelikely to involve the proximal part of small bowel withluminal constriction or even obstruction due to thehyperplasia of connective tissue of the bowel. Lym-phoma, on the other hand, primarily involves the termi-nal part of the small bowel rarely causing obstruction.‘Aneurysmal dilatation’ of the bowel wall is characteris-tically seen in lymphomas rather than carcinomas.24

Another lesion that can pose diagnostic challengeincludes Crohn’s disease affecting small bowel. Lesionsof Crohn’s disease are usually multiple and extensive,with the degree of bowel thickening and enlargement ofmesenteric lymph nodes being less pronounced than inlymphomas.20 Colonic carcinomas usually have lesionswith irregular border and regional lymph node enlarge-ment that rarely exceeds 2 cm in size. Lymphomas, on

L Zhu et al.


the other hand, usually have clear border, rarely invad-ing surrounding structures, and as other parts of the GItract have higher incidence of severe conglomerate lym-phadenopathy in the peritoneal cavity.27

Conclusion

PTCLs share some common features with B-cell type GIlymphomas while having some distinguishing radiologi-cal features. PTCLs usually present with multiplicity ininvolvement as well as with only mild or moderate thick-ening of the gastric or bowel wall and with a higherincidence of perforation. Unlike in Western population,GI PTCLs in Chinese population usually present in youngmales with colon as the preferential site with relativelyabsence of any enteropathy including CD.

Acknowledgement

The authors would like to thank Dr Jun Luo from pathol-ogy department for her expert advices.

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CT features of peripheral T-cell lymphoma in the gastrointestinal tract in Chinese population and...

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