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Gastrointestinal Lymphoproliferative Lesions: a Practical Diagnostic Approach

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Gastrointestinal Lymphoproliferative Lesions: a Practical Diagnostic Approach PATHOLOGICA 2020;112:227-247; DOI: 10.32074/1591-951X-161 Review Gastrointestinal lymphoproliferative lesions: a practical diagnostic approach Marco Pizzi1, Elena Sabattini2, Paola Parente3, Alberto Bellan4, Claudio Doglioni5, Stefano Lazzi6 1 General Pathology and Cytopathology Unit, Department of Medicine – DIMED, University of Padova, Italy; 2 Hematopathology Unit, Sant’Orsola University Hospital, Bologna (BO), Italy; 3 Pathology Unit, Fondazione IRCCS Ospedale Casa Sollievo della Sofferenza, San Giovanni Rotondo (FG), Italy; 4 Department of Pathology, ULSS6, Camposampiero Hospital, Camposampiero (PD), Italy; 5 Department of Pathology, University Vita- Salute San Raffaele, IRCCS San Raffaele Hospital, Milano, Italy; 6 Department of Medical Biotechnology, Section of Pathology, University of Siena, Italy Summary The gastrointestinal tract (GI) is the primary site of lymphoproliferative lesions, spanning from reactive lymphoid hyperplasia to overt lymphoma. The diagnosis of these diseases is challenging and an integrated approach based on clinical, morphological, immunohis- tochemical and molecular data is needed. To reach to confident conclusions, a stepwise approach is highly recommended. Histological evaluation should first assess the benign versus neoplastic nature of a given lymphoid infiltrate. Morphological and phenotypic anal- yses should then be applied to get to a definite diagnosis. This review addresses the key histological features and diagnostic workup of the most common GI non-Hodgkin lymphomas (NHLs). Differential diagnoses and possible pitfalls are discussed by considering distinct groups of lesions (i.e. small to medium B-cell NHLs; medium to large B-cell NHLs; T-cell NHLs; and mimickers of Hodgkin lymphoma). The key clinical and epidemiological features of each entity are also described. Received and accepted: June 29, 2020 Published online: 29 October, 2020 Key words: lymphoma, gastrointestinal lymphoma, Hodgkin lymphoma, B-cell lymphoma, T-cell lymphoma Correspondence Stefano Lazzi Department of Medical Biotechnology, Section of Pathology, University of Siena, via Introduction and clinical relevance delle Scotte 6, 53100 Siena (SI), Italy E-mail: [email protected] The gastrointestinal (GI) tract plays several immunologic functions, in- Conflict of interest cluding fine-tuning the intestinal microbiome, mediating tolerance toward The Authors declare no conflict of interest. food antigens and mounting immune responses against enteric patho- gens 1. Such functions rely on dedicated anatomical structures, widely How to cite this article: Pizzi M, Sabattini E, spread along the stomach, the small and large bowel (i.e. Peyer’s patch- Parente P, et al. Gastrointestinal lymphoprolif- es and rectal tonsil) 1,2. The physiologic and/or neoplastic expansion of erative lesions: a practical diagnostic approach. Pathologica 2020;112:227-247. https://doi. such structures gives rise to a broad spectrum of lesions, spanning from 3 org/10.32074/1591-951X-161 benign lymphoid hyperplasia to malignant B and T cell lymphomas . Gastrointestinal lymphoid proliferations are commonly found in the sur- © Copyright by Società Italiana di Anatomia Pato- gical pathology practice and their diagnosis can be challenging even logica e Citopatologia Diagnostica, Divisione Itali- ana della International Academy of Pathology for trained pathologists. This is due to their disguising and overlapping histological features, the small amount of diagnostic material and sam- OPEN ACCESS pling artifacts. Despite such limitations, histology is the gold standard for the diagnosis of GI lymphoproliferative disorders (LPDs) and guides This is an open access journal distributed in accordance 4 with the CC-BY-NC-ND (Creative Commons Attribution- the management of patients . For these reasons, when dealing with NonCommercial-NoDerivatives 4.0 International) license: the lymphoid infiltrates in the GI tract, every effort should be taken to get to work can be used by mentioning the author and the license, but only for non-commercial purposes and only in the original a diagnosis as accurate and informative as possible. version. For further information: https://creativecommons. This review will discuss the histological features of GI LPDs and org/licenses/by-nc-nd/4.0/deed.en non-Hodgkin lymphomas (NHLs), specifically addressing the key diag- 228 M. Pizzi et al. nostic features and pitfalls of each entity. A practical ical picture, the endoscopic findings and the severity approach will be followed, by grouping GI LPDs into of histological atypia. major diagnostic categories, discussing their general features and considering their differential diagnosis. This work is intended to support the surgical pathol- Primary GI lymphomas versus secondary ogy practice. For a detailed discussion of the clinical involvement by systemic disease and pathophysiological features of each entity, the reader is referred to the many excellent reviews pub- Once the neoplastic nature of a lymphoid infiltrate has lished on this topic 5-10. been established, another important issue is defin- ing its origin. The GI tract can indeed host both pri- mary NHLs and secondary localizations of systemic The diagnosis of GI LPDs: benign versus disease. The clinical criteria distinguishing these two malignant lesions groups of neoplasms were first proposed by Dawson in 1961. A NHL is considered of primary GI origin if, The first most compelling issue concerning GI LPDs at presentation: (i) peripheral and/or mediastinal lym- is to define whether they are benign or malignant in phadenopathies are lacking; (ii) blood cell counts are nature. Clues favoring a diagnosis of lymphoma over normal; (iii) the lesion is predominantly localized with- reactive lymphoid hyperplasia include: (i) tissue ef- in the GI tract and the only affected lymph nodes are facement by confluent sheets of lymphoid cells (even adjacent to such lesion; and (iv) the liver and spleen with polyp formation), (ii) infiltration and disruption of are spared 14. glandular units (i.e. “lymphoepithelial lesions”; LELs), By applying Dawson’s criteria, primary GI NHLs ac- (iii) atypical follicles, follicular colonization or expand- count for about 30-40% of all extra-nodal lymphomas ed mantle zones, (iv) the monomorphic composition and for 1-4% of GI malignancies 15. Secondary GI of the lymphoid infiltrate, and (v) the documentation of involvement is by far more frequent, being reported cytologically or phenotypically atypical elements, sin- in 5-20% of NHLs 16. The anatomic distribution of GI gly or in aggregate. None of these findings is pathog- NHLs varies across geographical areas: the stomach nomonic of lymphoma per se, nor all lymphomas dis- is primarily involved in Western countries 17, while close each of these features. It is rather the integration the small bowel is mostly affected in Middle East re- of multiple parameters that leads to a correct diagno- gions 18. In all, gastric and small intestinal NHLs ac- sis (Fig. 1). count for 80-85% of all GI cases. Molecular biology may also support the differential Primary GI NHLs are mostly of B-cell lineage (90% of diagnosis between reactive hyperplasia and lympho- cases), spanning from indolent to very aggressive ne- ma, the former being associated with polyclonal rear- oplasms. Peripheral T-cell lymphomas are less com- rangements of the immunoglobulin and T cell receptor mon and typically associated with poor prognosis. In genes, the latter showing monoclonal gene patterns. contrast to patients with known classic Hodgkin lym- Exceptions nonetheless exist to this rule. In fact, an- phoma (cHL), great caution is required before making tigen-driven monoclonal populations are commonly a diagnosis of primary cHL in extranodal sites (stage found in inflammatory, infectious or autoimmune re- IE is extremely rare: 0.25-1% of cases). Mimickers of sponses 11 and polyclonal patterns may characterize cHL are well documented and will be addressed in highly mutant NHLs, as a result of limited primer an- a separate section of this review. Finally, the GI tract nealing and poor amplification of the monoclonal se- is frequently site of post-transplant LPDs (PTLDs). quences 12. Thus, the finding of a monoclonal peak These lesions are frequently driven by EBV infection does not necessarily imply a diagnosis of lymphoma and include benign, non-destructive lymphoid or plas- and the results of molecular biology should always be ma cell proliferations (i.e. follicular hyperplasia, plas- integrated with the clinical-pathological findings. ma cell hyperplasia, infectious mononucleosis-like Despite extensive phenotypic and molecular charac- LPDs), polymorphic and monomorphic B and T/NK- terization, in a minority of cases a definite diagnosis cell PTLDs (Tab. I). cannot be made. In such instances, the degree of un- certainty should be stated in the pathology report and NON-HODGKIN B CELL LYMPHOMAS OF THE GI TRACT provisional statements of “atypical lymphoid hyperpla- For diagnostic purposes, B-cell NHLs can be grouped sia/infiltrates”, “lymphoid infiltrate of uncertain poten- in two broad disease categories: (i) tumors consisting tial/significance”, or “lymphoid infiltrate suspicious but of small to medium size B-cells; and (ii) tumors con- not certain for lymphoma” may be proposed 13. The sisting of medium to large size B-cells. The first group management of such lesions will depend on the clin- encompasses extra-nodal marginal zone lymphoma DIAGNOSIS OF GI LYMPHOPROLIFERATIVE DISORDERS 229 Figure 1. Differential
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