Resident Short Review
Duodenal-Type Follicular Lymphoma
A Clinicopathologic Review
Etan Marks, DO; Yang Shi, MD, PhD
 Duodenal-type follicular lymphoma (D-FL) is a newly
recognized entity in the 2016 World Health Organization
classification update. It has an immunophenotype similar
to that of other FLs and usually carries the typical
t(14;18)(q32;q21) translocation. However, unlike other
FLs, D-FL is almost always diagnosed at a low stage and
stays localized to the small intestine, most commonly the
second portion of the duodenum, whereas the vast
majority of other FLs are diagnosed at an advanced stage.
Additionally, D-FL gene expression and pathogenesis
appear to be more closely related to extranodal marginal
zone lymphoma of mucosa-associated lymphoid tissue
than to other types of FL. Therefore, many oncologists have
opted to treat this variant of FL in a ‘‘watch and wait’’
manner because of its excellent prognosis and the rarity of
D-FL to progress even when no treatments are attempted.
(Arch Pathol Lab Med. 2018;142:542–547; doi: 10.5858/
arpa.2016-0519-RS)
F ollicular lymphoma (FL) is the second most common
type of non-Hodgkin lymphoma in the United States.1
It is graded by using the number of centroblasts per 340
high-power field (hpf; hpf ¼ 18-mm field of view) as grading
criteria2: grade 1 is 5 or fewer centroblasts per hpf; grade 2 is
6 to 15 centroblasts per hpf; and grade 3 is more than 15
centroblasts per hpf. Grade 3 is further subdivided into 3A
(centrocytes still present) and 3B (sheets of centroblasts).3
Follicular lymphoma grades 1 and 2 have been combined
into one entity because both are considered to have an
indolent course.
As common as FL is, it only accounts for approximately
4% of gastrointestinal (GI) lymphomas.1,4–6 Of these, it is
interesting to note that a large percentage (between 38%
and 81%) arise in the duodenum.7–9 The FLs of this site are
commonly localized to the intestine without nodal metas-
tasis,9 similar to how primary cutaneous follicle center
lymphoma stays localized to the skin.10 Conversely, the vast
Accepted for publication February 7, 2017.
From the Department of Pathology, Montefiore Medical Center/
Albert Einstein College of Medicine, Bronx, New York.
The authors have no relevant financial interest in the products or
companies described in this article.
Reprints: Etan Marks, DO, Department of Pathology, Montefiore
Medical Center/Albert Einstein College of Medicine, 111 E 210th St,
Bronx, NY 10467 (email: emarks@montefiore.org or et565@aol.
com).
542 Arch Pathol Lab Med—Vol 142, April 2018
majority of patients presenting with FLs at other sites are at
an advanced stage of disease.1,11 This has led the World
Health Organization to recognize this entity as a distinct
form of FL—duodenal-type follicular lymphoma (D-FL)—in
its 2016 update.12
CLINICAL FEATURES
Most D-FLs are detected incidentally, with endoscopy
being done for reasons unlikely to be related to the D-FL,
because low-stage FLs rarely cause clinical symptoms. This
is most likely why FLs are detected at advanced stages in the
vast majority of cases. In a study performed in Europe by
Schmatz et al,9 the patients usually either had some type of
upper GI symptoms, the D-FL was discovered while staging
for other types of malignancies, or the endoscopy was part
of a preventative medical examination. However, in another
study performed in Japan by Takata et al,8 the vast majority
of patients presented with no symptoms, and only a small
cohort had some form of abdominal symptoms. Neither
study revealed a predilection for either sex, and the median
age for each study was 65 and 59 years, respectively. In the
Takata et al8 study, 97 of 99 patients (98%) with involvement
of the second portion of the duodenum had a 5-year
progression-free survival. This is compared with only 19 of
27 patients (70%) without involvement of the second
portion of the duodenum who had a 5-year progression-
free survival.
Regarding disease staging, although Ann Arbor staging is
more commonly used for FL of other sites, it appears that
the International Workshop classification (Lugano classifi-
cation) is more appropriate for the clinical staging of D-FL.
The reason for this is that the Lugano staging criteria are
commonly used for GI lymphoma staging and, because of
the multifocal nature of D-FL, it is more similar to other GI
lymphomas rather than the FLs of other sites. The Takata et
al8 and Schmatz et al9 studies both used the Lugano staging
criteria, and of the 162 patients, none were higher than a
stage II.
ENDOSCOPIC FINDINGS
The lesions of D-FL usually appear as solitary or multiple
nodules (Figure 1), or polypoid lesions, and are usually
between 1 and 5 mm. These lesions can become ulcerated,
and in that situation it is important to biopsy the
surrounding area for a better diagnostic yield. They can be
located anywhere in the duodenum, but the second portion/
descending part is by far the most common area. These
Duodenal-Type Follicular Lymphoma—Marks & Shi
Figure 1. Endoscopic picture reveals a nodularity. The arrow points to the nodularity. The arrowheads indicate the border of the nodularity.
Figure 2. Follicular lymphoma presents as enlarged follicles without a mantle zone. The lymphoma cells are found outside of the follicles and in the
villi (hematoxylin-eosin, original magnification 34).
Figure 3. The lymphoma consists of predominantly small neoplastic lymphocytes with slightly irregular nuclear contours (hematoxylin-eosin,
original magnification 340).
Figure 4. CD20 immunohistochemistry stain reveals that the lymphocytes are predominantly of B-cell lineage (original magnification 34).

lesions can occur in other areas of the small intestine, such
as the jejunum and the ileum, along with the duodenum.8,9
In fact, multifocal disease in the small intestine is not
uncommon, with 1 large series showing multiple lesions
occurring in 49 of 63 cases (78%), and lesions located in the
jejunum or ileum along with the duodenum in 11 of 63 cases
(18%).9 In another large study, Takata et al8 found that, of
the patients with D-FL in the second portion of the
duodenum, only 8 of 54 patients (15%) had localized
tumors, whereas the remaining 46 patients (85%) had
involvement in other areas of the intestine, mainly the
jejunum.
HISTOLOGY AND ANCILLARY STUDIES
Unlike other FLs, D-FL is usually a low-grade lesion
(grades 1–2), with 1 study showing grades 1 to 2 in all 54
patients with second portion of the duodenum involve-
ment,8 and another study showing grades 1 to 2 in all 63
patients with D-FL.9 The possibility of high-grade transfor-
Arch Pathol Lab Med—Vol 142, April 2018
mation is extremely rare but possible, because Mori et al13
reported that 1 of 27 patients (3%) developed histologic
transformation to grade 3A. Usually, D-FL appears as
several well-circumscribed germinal centers packed togeth-
er with centrocytes and few, if any, centroblasts with no
visible tingible body macrophages and without mantle
zones. Sheets of small lymphoid cells with irregular nuclear
contour are usually present outside the follicular structures,
and the lymphoma usually involves the mucosa and
submucosa. The neoplastic cells commonly involve duode-
nal villi (Figures 2 and 3). This is in contrast to other GI-FLs,
which are commonly found between the submucosal and
the subserosal areas.14
The neoplastic cells show an immunophenotype similar to
that of low-grade nodal FL (NFL) by expressing CD20
(Figure 4), CD79a, CD10 (Figure 5), BCL-6, BCL-2 (Figure
6), and BACH2, and show a lack of expression for CD5,
CD23, CD43, BCL-1 (cyclin D1), MUM-1, Blimp-1, and T-
cell markers.9,14 They also show a low Ki-67 proliferation
Duodenal-Type Follicular Lymphoma—Marks & Shi 543
Figure 5. CD10 immunohistochemistry stain reveals that the small lymphocytes in and between the follicles are of follicular origin (original
magnification 310).
Figure 6. BCL2 is aberrantly expressed on the neoplastic cells (original magnification 34).
Figure 7. The tumor has a low proliferation rate, as seen with Ki-67 immunohistochemistry stain (original magnification 310).
Figure 8. CD21 reveals that the follicular dendritic mesh work is located in the peripheral part of the follicles (original magnification 320).

rate (Figure 7). However, D-FL shows a different pattern of
CD21 (Figure 8) and CD23 expression of the follicular
dendritic cells (FDCs) in the germinal center compared with
NFL and compared with FL found at other extranodal sites,
including those of the colon and stomach. Usually, NFLs
and other extranodal FLs will have an FDC network that
occupies more than two-thirds of the neoplastic germinal
centers. In D-FL, the FDCs are located at the periphery and
occupy less than 10% of the neoplastic germinal cen-
ter.8,9,14,15 It is interesting to note that Takata et al15 showed
that FL cells interact with the FDCs of the germinal center,
and FDCs give a growth advantage to the lymphoma cells.
Therefore, the lack of FDCs and this interaction with the
neoplastic FL cells may help explain the low-grade behavior
of the D-FL.
PATHOGENESIS AND GENETIC FEATURES
The hallmark genetic aberration found in most FLs is the
t(14;18)(q32;q21) translocation of the genes immunoglobu-
lin heavy chain (IGH) and B-cell leukemia/lymphoma 2
544 Arch Pathol Lab Med—Vol 142, April 2018
(BCL2).16,17 This translocation is present in most cases of D-
FL, confirming that this lymphoma is part of the FL
family.9,13–15 However, unlike most FLs, D-FL appears to
have a unique pathogenesis that is related to inflammation
and antigen stimulation, and shares some similarities with
mucosa-associated lymphoid tissue (MALT) lymphoma.
Regarding the immunoglobulin variable region heavy-
chain (IgVH) gene rearrangements, D-FLs show a higher
use of VH4 and VH5 than nodal cases.14,15,18 Also, in 1 study
VH4-34 and VH5-51 were detected in 3 samples each.15 This
selective use suggests that some antigen-dependent mech-
anism is involved in tumor development, similar to MALT
lymphoma, which develops from chronic inflammation. In
fact, there have been reports of D-FL where regression has
occurred following eradication of the Helicobacter pylori
organisms.19
Duodenal-type FL shows expression that differs from that
of GI-FL with regard to CD27 and activation-induced
cytidine deaminase (AID). CD27 shows positivity in D-FL,
whereas AID is negative and the inverse is true for GI-FL.14
Duodenal-Type Follicular Lymphoma—Marks & Shi
CD27 is a type 1 glycoprotein, a member of the tumor
necrosis factor receptor family, and a marker for memory B
cells.20 AID is a member of the RNA-editing cytidine
deaminase family, which is specifically expressed in
germinal center B cells, has been shown to be necessary
for B-cell class switching, and is involved in hypermuta-
tion.21
Takata et al22 undertook the task of creating a gene
expression profile for D-FL, using 10 cases, and compared it
to the gene expression of 10 gastric MALT lymphomas, 18
NFLs, 5 normal duodenal mucosae, 8 nodal reactive
lymphoid hyperplasias, and 4 normal gastric mucosae. After
analyzing whole-genome expression data, they selected
2918 genes that were either upregulated or down-regulated
to study the differentially expressed genes. They found that
compared with the normal duodenal mucosa group, the top
5 upregulated genes in D-FL were the complement receptor
2, chemokine ligand 4 (CCL4), cannabinoid receptor 2, T-
cell activation Rho GTPase-activating protein, and interleu-
kin 21. The top 5 down-regulated genes were glutathione
peroxidase 3, CDKN2B (p15), phospholipase A2 receptor 1,
plasminogen activator, and diacylglycerol lipase.
In order to validate the expression profiles observed in the
gene expression profile, immunohistochemistry was pur-
sued for chemokine (C-C motif) ligand 20 (CCL20), CCR6,
mucosal vascular addressin cell adhesion molecule 1
(MAdCAM-1), and protocadherin gamma A3 (PCDHGA3),
A8 (PCDHGA8), and B4 (PCDHGB4). All of these genes
were upregulated in D-FL and stained positive with
immunohistochemistry in the D-FL cells.22 CCL20 (also
known as macrophage inflammatory protein 3a) is a
chemokine expressed in follicle-associated epithelium, and
CCR6, its only known receptor, is highly expressed in
human dendritic cells.23,24 MAdCAM-1 is an immunoglob-
ulin (Ig) family member with domains that display
homologies to mucosa-associated Ig family members, and
it appears to be important for regulating lymphocyte
homing to mucosal sites.25 PCDHGA3, PCDHGA8, and
PCDHGB4 represent a prominent gene family that encodes
cell-cell adhesion proteins.
The above findings show that D-FLs share similar gene/
protein expression profiles with both MALT lymphoma and
NFL. With regard to the CCL20, CCR6, and MAdCAM-1
gene expression profiles, D-FL is similar to MALT lympho-
ma, and it was hypothesized that increased expression of
CCL20 and MAdCAM-1, along with coexpression of CCL20
and CCR6, might play an important role in tumorigenesis.
However, with regard to PCDHGA3, PCDHGA8, and
PCDHGB4 gene expression profiles, D-FL is similar to NFL.
DIFFERENTIAL DIAGNOSIS
Duodenal-type FL, because of its histologic low grade and
indolent behavior, can be confused with several different
lymphoid entities, such as reactive follicular hyperplasia,
MALT lymphoma, chronic lymphocytic leukemia/small
lymphocytic lymphoma, mantle cell lymphoma, and GI
involvement by systemic FL.
Reactive follicular hyperplasia may have many follicles
with germinal centers, but they usually vary in size and
shape, have tingible body macrophages, have polarized
germinal centers, and have preserved dendritic cell mesh-
work, and the interfollicular lymphocytes will differ from the
follicular lymphocytes. The secondary follicles will stain for
BCL-6 and CD10, but not for BCL-2. MALT lymphoma is
Arch Pathol Lab Med—Vol 142, April 2018
more common in the stomach than the small bowel. In low-
grade lesions it is made up of small lymphocytes with
irregular nuclei, and reactive germinal centers are common.
It is often negative for CD5, CD10, and BCL-6, because it is
derived from post–germinal center memory B cells. Some
lymphoma cells can aberrantly express CD43, and the most
common genetic aberration is a t(11;18). Chronic lympho-
cytic leukemia/small lymphocytic lymphoma is commonly
associated with lymphadenopathy or splenomegaly. When
there is prominent lymphocytosis in chronic lymphocytic
leukemia/small lymphocytic lymphoma, the neoplastic
lymphocytes can be seen all over the body, including in
the GI system. The architecture is effaced by sheets of small
B cells with clumped chromatin and scant cytoplasm. CD5 is
usually positive, but there is no expression for CD10 or BCL-
6, and CD20 might be dimly expressed. Moreover, lymphoid
enhancer-binding factor 1 (LEF1) is almost always positive
in chronic lymphocytic leukemia/small lymphocytic lym-
phoma.
Mantle cell lymphoma can sometimes involve the GI tract
and present as polyps. The infiltrate often appears nodular,
can involve the lamina propria, and can have scalloped
edges. The lymphoid cells are small, round, and monoto-
nous, resemble centrocytes, and often infiltrate between
glands instead of replacing them. The cells will show
positivity for CD20 and CD5, but cyclin D1 positivity will be
the most helpful in identifying this lesion, which correlates
with the common t(11;14) present in this entity. Nodal FL
will often present with generalized lymphadenopathy and
bone marrow involvement. Occasionally, it can also involve
the GI system. Histologically, it will appear very similar to
D-FL when it is grades 1 to 2, but the staining pattern of
CD21 of the germinal centers will be more diffusely positive
in NFL compared with D-FL. Therefore, performing a
thorough physical examination and a detailed radiologic
investigation, including a positron emission tomography–
computed tomography scan to rule out GI involvement by a
systemic FL, is critical before a diagnosis of primary D-FL is
rendered.
In general, D-FL can be differentiated from a reactive
follicular hyperplasia and the other small B-cell lymphomas
in several ways. First, the histology shows prominent
follicles that lack tingible body macrophages and polariza-
tion. It shows expression of CD20, CD10, and BCL-6,
revealing a germinal center origin, but it also expresses
BCL-2, revealing its aberrant nature. Additionally, the
t(14;18) was shown to be present by fluorescent in situ
hybridization or conventional cytogenetics in 15 of 16 cases
(93.8%) by Schmatz et al,9 and in 13 of 15 cases (86.7%) by
Takata et al,14 overall being present in 90% of cases, and this
can help diagnose a D-FL. Lastly, in most cases, D-FL is
confined to the small intestine.
TREATMENT AND CLINICAL OUTCOME OF THE
DISEASE
Follicular lymphoma is considered an indolent lymphoma
with a fairly good prognosis, with median overall survival
exceeding 12 years, but it is considered incurable with
standard chemotherapy.26 Unlike FLs at other anatomic
sites, D-FL is usually a low-grade lesion (grades 1–2) and
mainly presents at a low stage. It is often an indolent
disease, and its prognosis is similar to that of FL/neoplasia
in situ.
Duodenal-Type Follicular Lymphoma—Marks & Shi 545
 Differences Between Duodenal-Type Follicular Lymphoma (D-FL), Nodal Follicular Lymphoma (NFL),
and Gastrointestinal Follicular Lymphoma (GI-FL), Not of the Duodenum
D-FL NFL GI-FL
Grade 1–2a 1–2 or 3 1–2 or 3
Stage at presentationb I or II III or IVc I–IV
BCL-6 þ þ þ
CD10 þ þ þ
BCL-2 þ þ þ
AID  þ þ
CD21 Peripheral of GC (duodenal pattern), Dense in GC (nodal pattern), Dense in GC (nodal pattern),
10% of follicle 67% of follicle 67% of follicle
CD27 þ þ 
MUM1   
Blimp-1   
t(14;18) ~90% 60%–90% 60%–90%
IgVH use VH3, VH4, VH5 VH3, most cases VH3, most cases
Abbreviations: AID, activation-induced cytidine deaminase; Blimp-1, B-lymphocyte maturation protein 1; GC, germinal center; IgVH,
immunoglobulin heavy-chain variable genes; þ, positive; , negative.
a
The vast majority of D-FLs are of grades 1–2. However, very rare cases that transformed to high-grade B-cell lymphoma have been reported.
b
D-FL staging was by the Lugano classification; NFL and GI-FL staging was by the Ann Arbor classification.
c
Most NFLs present at stages III–IV, although a minority of cases can present at a lower stage.

Patients with limited-stage FLs treated with radiation CONCLUSIONS

therapy, usually external beam radiation therapy, have
shown a long disease-free survival following therapy, with
an overall survival rate of 60% to 80% at 10 years.27,28
Therefore, it is possible that in some instances of limited
disease, radiation therapy leads to a cure. This is especially
true because if a patient has not relapsed within the first 10
years, he or she is unlikely to relapse at all.29 This has led to
radiation therapy being the treatment of choice for limited-
stage disease for more than 4 decades.30 However, 1 study
showed that among patients who received radiation
therapy, 47 of 98 (48%) relapsed.28 Among patients who
relapse, progression-free survival at 10 years is 22%.31
Therefore, chemotherapy has been added to some regimens
and demonstrated an improved progression-free survival
without an effect on overall survival.26
Even with the success of radiotherapy, in the United
States patients with stage I disease are treated with this
modality less than 50% of the time, at least initially. Many
oncologists in the United States initially take a ‘‘watch and
wait’’ approach, which has been shown to be equally
effective.32 The other approaches for early-stage disease
consist of rituximab-chemotherapy, rituximab alone, com-
bined modality therapy, other chemotherapies, or other
therapy.26
In a retrospective study of 63 patients with D-FL, the
treatment modalities were watchful waiting only (24;
41%), radiotherapy (19; 33%), rituximab monotherapy (5;
9%), cyclophosphamide, doxorubicin, vincristine, predni-
sone (CHOP; 2; 3%), rituximab plus CHOP (2; 3%),
radiotherapy and rituximab (1; 2%), other chemotherapy
protocols (3; 5%), and Whipple procedure (2; 3%); 5
patients had no control endoscopy and were not included
in the therapy discussion.9 Patients in each treatment
group showed complete regression in 7 of 24 (29%), 19 of
19 (100%), and 4 of 5 (80%) in the first 3 groups, and 5 of 8
(63%) in the following 4 groups combined (chemotherapy
with or without radiation), respectively. The authors
found only 2 of 63 patients (3%) had dissemination to
nodal sites 5 years after initial diagnosis, and both were in
the ‘‘watch and wait’’ group, but the remaining 61 of 63
patients (97%) did not develop lymphoma outside the
small bowel.
Duodenal-type FL is a unique subtype of FL. Clinically,
immunophenotypically, and genetically it is different from
NFL (Table) and shares many characteristics with MALT
lymphoma. However, it morphologically resembles a low-
grade FL (FL1-2) and expresses BCL-2, probably because it
has the unique t(14;18) that is characteristic of FLs in
general. In the United States most oncologists either take a
‘‘watch and wait’’ approach, or they treat with radiotherapy.
More recently, some oncologists have chosen rituximab or
even opted for chemotherapy. However, most do not
choose chemotherapy because of the good prognosis of
D-FL and the toxic side effects of chemotherapy.
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