Hematopathology / HODGKIN LYMPHOMA INVOLVING WALDEYER RING

Hodgkin Lymphoma Involving Waldeyer Ring

A Clinicopathologic Study of 22 Cases
Maria del Pilar Quiones-Avila, MD, Abel A. Gonzalez-Longoria, MD, Joan H. Admirand, MD,
and L. Jeffrey Medeiros, MD
Key Words: Hodgkin lymphoma; Waldeyer ring; Epstein-Barr virus
DOI: 10.1309/33YCNMW08KNA36NT

We report 22 cases of Hodgkin lymphoma involving

Waldeyer ring seen at our institution during a 31-year
interval. There were 16 males (73%) and 6 females
(27%) with a median age of 48 years (range, 5-81
years), and 15 (68%) patients had airway obstruction
or tonsillar enlargement. For 19 patients, the clinical
stage was as follows: I, 7 (32%); II, 11 (50%); and III,
1 (5%). The 3 patients (14%) whose disease was
unstaged had concurrent or a history of non-Hodgkin
lymphoma. Histologically, the neoplasms were
classified as follows: lymphocyte-rich classical, 8
(36%); nodular sclerosis, 7 (32%); mixed cellularity, 4
(18%); unclassified, 2 (9%); and lymphocyte depletion,
1 (5%). Of 7 stage I cases, 4 (57%) were the
lymphocyte-rich classical type. Reed-Sternberg and
Hodgkin cells were positive for CD15 and CD30 in 20
cases assessed. Epstein-Barr virus latent membrane
protein type 1 was positive in 12 (67%) of 18 cases
assessed. We conclude that Hodgkin lymphoma rarely
involves Waldeyer ring, with the lymphocyte-rich
classical type being common at this location.

The term Waldeyer ring is used to encompass the lymphoid

tissues of the faucial tonsils, nasopharynx, base of tongue, and
oropharynx and, as defined by others, is an extranodal but not an
extralymphatic site.1 Waldeyer ring may be involved by a variety
of neoplasms, and carcinomas, most often metastatic from nearby head and neck sites, are most common. Lymphomas involve
Waldeyer ring much less often,2 and most of these tumors are
non-Hodgkin lymphomas (NHLs). In published studies, approximately 90% of all lymphomas involving Waldeyer ring are
types of NHL,3 mostly extranodal natural killer/T-cell lymphoma of nasal type and diffuse large B-cell lymphoma,4-6 with
a lesser number of other types, including extranodal marginal
zone B-cell lymphoma of mucosa-associated lymphoid tissue,
mantle cell lymphoma, and peripheral T-cell lymphoma.
Hodgkin lymphoma (HL) represents approximately 4% of
all lymphomas of the head and neck,7 and most of these neoplasms involve lymph nodes. Extranodal involvement by HL,
including Waldeyer ring, is rare.4,5 Previous studies of patients
with HL have reported a low frequency of involvement of
Waldeyer ring. For example, Todd and Michaels8 reported a
frequency of 1% for involvement of the nasopharynx and 1.5%
for tonsil and oropharynx. Similarly, Kaplan and colleagues9
reported that 5 (1.8%) of 285 consecutive patients with HL had
involvement of Waldeyer ring. As a result, most previously
published series of HL involving Waldeyer ring have been
small groups of patients or case reports. In addition, most of
the larger and better studies were performed before the advent
of immunohistochemical analysis and, therefore, lack confirmatory immunophenotypic data. Most of these studies also
used older lymphoma classification systems based on morphologic findings, without ancillary data. A study of a series
of cases of HL involving Waldeyer ring, classified according
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Abstract

Quiones-Avila et al / HODGKIN LYMPHOMA INVOLVING WALDEYER RING

to the currently used World Health Organization (WHO) classification system, has not been published to date.
We describe 22 cases of HL involving Waldeyer ring,
including 7 stage I cases, classified according to the WHO
classification.

Carpinteria, CA, except CD15, which was purchased from BD

Biosciences, San Jose, CA.
All cases were classified using the criteria of the WHO
classification system.12 Although similar to earlier classifications of HL, the lymphocyte-rich classical type of HL now is
recognized as an entity in the WHO classification.

Materials and Methods

Results
Clinical Findings
Clinical data are summarized in Table 1. There were 16
males (73%) and 6 females (27%) with a median age of 48
years (range, 5-81 years). Only 1 patient (5%) was a child. Six
patients (27%) were at least 60 years old. The disease was
localized (stage I) to Waldeyer ring in 7 cases (32%), involved
Waldeyer ring and cervical lymph nodes (stage II) in 11 cases
(50%), and was associated with abdominal lymphadenopathy
and spleen involvement (stage III) in 1 case (5%).
Three patients had a history of NHL, and their disease was
not staged. In this subgroup, 1 patient had follicular lymphoma
with bone marrow involvement diagnosed in 1989 and was
treated with chemotherapy and autologous bone marrow transplantation. The patient experienced a relapse in 1992 with bone
marrow involvement by follicular lymphoma but was in clinical remission when HL developed in 1993 with involvement of
the mediastinum and liver. Despite chemotherapy, HL involving the bone marrow and then tonsil developed in 1994. Two
patients had chronic lymphocytic leukemia/small lymphocytic

Table 1
Clinical Features in 22 Cases of Hodgkin Lymphoma in Waldeyer Ring
Case No./Sex/
Age (y)
1/M/45
2/M/45
3/F/47
4/M/49
5/M/39
6/F/71
7/M/81
8/F/32
9/M/69
10/M/37
11/M/32
12/M/53
13/M/53
14/M/24
15/M/57
16/F/67
17/M/5
18/M/41
19/M/48
20/F/57
21/M/70
22/F/80

Biopsy Site
Nasopharynx and LN
Nasopharynx and LN
Nasopharynx
Tonsil
Tonsil, cervical and celiac LNs, spleen
Nasopharynx
Tonsil
Adenoid and LN
Nasopharynx and LN
Adenoid
Tonsil
Tonsil and LN
Nasopharynx
Nasopharynx
Nasopharynx
Nasopharynx and LN
Nasopharynx and LN
Adenoids
Adenoids and cervical LN
Mediastinum and LN
Tongue and LN
Palate, buccal gingiva

Symptoms and/or Signs

Right-sided neck mass
Nasal stuffiness
Nasopharyngeal mass
Tonsil enlargement
Tonsil enlargement
Nasopharyngeal mass
Tonsil enlargement
Right-sided neck mass
Cervical adenopathy
Nasal congestion; LN enlargement
Throat pain
Tonsil enlargement
Nasopharyngeal mass
Mass in sinuses (HIV+)
Nasopharyngeal mass
Nasopharyngeal mass; LN enlarged
Difficulty breathing
Obstructed airway
Nasal stuffiness
Mediastinal mass; painful throat
Exophytic lesion, base of tongue
Pain in the mouth; ulcers

Clinical Stage

History of
Lymphoma

II
II
I
II
III
II
I
II
II
II
I
II
I
I
I
II
II
I
II

+
+
+

LN, lymph node; +, positive; , negative.

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We identified 22 cases of HL involving Waldeyer ring in

the files of the Department of Hematopathology, The
University of Texas M.D. Anderson Cancer Center, Houston,
from January 1973 to December 2004. Eleven cases were
treated at this institution and 11 cases were reviewed in consultation. Clinical information was obtained from data submitted at the time of consultation and the medical record. Clinical
stage was determined using the Ann-Arbor staging system.
We reviewed H&E-stained tissue sections of each case.
We also reviewed all immunostains available, performed at
the submitting institution or in our laboratory in the past.
Immunohistochemical stains also were performed as part of
this study, using fixed, paraffin-embedded tissue sections and
an avidin-biotin complex method as previously described.10,11
The panel of monoclonal antibodies used included reagents
specific for CD15 (Leu M1), CD20 (L-26), CD30 (Ber H2),
CD45 (LCA), CD45RO (UCHL-1), Epstein-Barr virus (EBV)
latent membrane protein type 1 (LMP-1; CS1-4), and polyclonal CD3. Antibody dilutions varied during the interval of
the study. All antibodies were obtained from DAKO,

Hematopathology / ORIGINAL ARTICLE

lymphoma (CLL/SLL). One patient had fatigue and tenderness

and pain in the mouth related to ulcers. Biopsies of the palate
and buccal gingiva showed classical HL, and the patient underwent bone marrow aspiration and biopsy for staging. The bone
marrow and flow cytometric immunophenotypic studies
showed involvement by CLL/SLL without HL. The other
patient had a 5-year history of CLL/SLL that was treated with
chemotherapy. The patient was in clinical remission when an
exophytic lesion at the base of the tongue and bilateral enlarged
cervical lymph nodes developed. A biopsy of the tongue
revealed classical HL and CLL/SLL Image 1E.

Discussion
Although HL often involves the head and neck, these neoplasms usually arise in lymph nodes, most frequently in the cervical regions, and extranodal manifestation without nodal
involvement is rare.4,7 The frequency of HL involving extranodal
sites of the head and neck is approximately 4%.7 Among this
group, HL involving Waldeyer ring, which encompasses the
lymphoid tissues of the tonsils, nasopharynx, base of the tongue,
and oropharynx wall, is even more rare.3,6,13-21 For the present
study, we identified 22 cases of HL involving Waldeyer ring
obtained from the files of our institution during a 31-year period.
Although previous studies of HL involving Waldeyer ring
can be found in the literature, many of these studies did not
include immunohistochemical data. For example, the largest
series in the literature, by Cionini et al,13 was a group of 28 cases

Table 2
Pathologic and Immunophenotypic Findings in 22 Cases of Hodgkin Lymphoma in Waldeyer Ring
Case No.
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22

Diagnosis

CD3

CD15

CD20

CD30

CD45

CD45RO

EBV LMP-1

MC
NS
LRC
NS
MC
MC
NS
LRC
LRC
LRC
MC
NS
LRC
LD
LRC
NS
NS
LRC
LRC
NS
RS-HL
RS-HL

ND
ND

ND
ND
ND
ND

ND

ND
ND

+
+
+
ND
+
+
ND
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+

ND
ND

ND
ND

+
+

+
+
+
ND
+
+
ND
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+

ND
ND

ND

ND

ND

ND
ND

ND

ND
ND
ND
ND
ND
ND
ND
ND

ND
ND
ND
ND
ND
ND
ND
ND
ND

ND
ND

+
ND
+
+
ND
+

+
+

+
+
ND
ND
+

+
+
+

EBV LMP-1, Epstein-Barr virus latent membrane protein type 1; LD, lymphocyte-depleted; LRC, lymphocyte-rich classical; MC, mixed cellularity; ND, not done; NS, nodular
sclerosis; RS-HL, Richter syndrome, Hodgkin lymphoma type; +, positive; , negative.

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Pathologic and Immunohistochemical Findings

Pathologic and immunohistochemical data are summarized in Table 2. According to the WHO classification criteria, all 22 cases were classified as classical HL and 20 cases
were further classified as follows: lymphocyte-rich classical
Image 1A and Image 1B, 8 (36%); nodular sclerosis Image
1C, 7 (32%); mixed cellularity, 4 (18%); and lymphocyte
depletion, 1 (5%). The remaining 2 cases (9%) arose in patients
with CLL/SLL (Image 1E) and therefore were not further classifiable. The 7 stage I cases were classified as follows: lymphocyte-rich classical, 4 (57%); mixed cellularity, nodular sclerosis, and lymphocyte depletion, 1 (14%) each.
In 20 cases, immunohistochemical studies were performed. (These studies were not performed in 2 cases of nodular sclerosis.) In all cases, the Reed-Sternberg and mononuclear
variant cells were positive for CD15 and CD30 Image 1D.
EBV LMP-1 was positive in 12 (67%) of 18 cases assessed,

and CD20 was variably positive in 5 (28%) of 18 cases

assessed. The neoplastic cells were negative for CD45 (n = 14),
CD3 (n = 13), and CD45RO (n = 3) in all cases assessed.
The 12 cases positive for EBV LMP-1 were classified as
follows: lymphocyte-rich classical, 4 (33%); mixed cellularity, 3 (25%); nodular sclerosis, 2 (17%); lymphocyte depletion,
1 (8%); and not classified, 2 (17%) Image 1F. The patient
with lymphocyte depletion HL was HIV+. The clinical stage
of the neoplasms in these patients was as follows: I, 4; II, 4;
III, 1; and not staged, 3. The 3 patients with unstaged disease
had concurrent or a history of NHL.

Quiones-Avila et al / HODGKIN LYMPHOMA INVOLVING WALDEYER RING

Image 1 Hodgkin lymphoma involving Waldeyer ring. A, Lymphocyte-rich classical Hodgkin lymphoma involving adenoid tissue.
Note the nodular growth pattern similar to that seen in nodular lymphocyte-predominant Hodgkin lymphoma (H&E, 50). B,
Typical binucleated Reed-Sternberg cell in lymphocyte-rich classical Hodgkin lymphoma (H&E, 400). C, Nodular sclerosis
Hodgkin lymphoma involving tonsil. Fibrous collagen bands divide the tissue into nodules (H&E, 100). D, Typical membranous
and Golgi pattern of CD30 immunohistochemical staining in Hodgkin cells of nodular sclerosis Hodgkin lymphoma (400).

without immunophenotypic workup. Because various types of

NHL can resemble HL, such as T-cell/histiocyte-rich large Bcell lymphoma and peripheral T-cell lymphoma, immunohistochemical confirmation is needed to establish the diagnosis of
most types of HL, with the possible exception of nodular sclerosis. Another drawback of many previous studies is that older
lymphoma classification systems were used. Many of these
older classification systems were based purely on morphologic
findings and did not incorporate immunohistochemical and
other ancillary data. As far as we are aware, this is the first study
of a series of HL cases involving Waldeyer ring in which the neoplasms are classified according to the WHO classification.12
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Most reports in the literature suggest that mixed cellularity is the most common type of HL involving Waldeyer
ring,3,14-18 although the study by Cionini et al13 found that
lymphocyte predominant HL was most common. Our results
are in disagreement with the literature because we had a predominance of the lymphocyte-rich classical (8/22 [36%]) and
nodular sclerosis (7/22 [32%]) types of HL. In addition, more
than half of localized (stage I) cases were the lymphocyte-rich
classical type. This may be attributable, in large part, to the
fact that the category of lymphocyte-rich classical HL was not
recognized until it was first proposed as a provisional entity in
the Revised European-American Lymphoma classification in
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Hematopathology / ORIGINAL ARTICLE

1994.22 Furthermore, lymphocyte-rich classical HL was

refined into nodular and diffuse variants relatively recently, by
the European Task Force on Lymphoma project.23 Many cases
classified in the past as mixed cellularity, nodular lymphocyte
predominant, or unclassifiable HL might, in retrospect, be better considered the lymphocyte-rich classical type using current terminology and immunohistochemical analysis.23
Extranodal HL frequently is related to immunodeficiency
states, and in affected patients, a variety of anatomic sites can be
involved by HL, including Waldeyer ring.24,25 Thus, immunodeficiency is one possible explanation for involvement of
Waldeyer ring by HL in the 4 patients with a history of lymphoma (n = 3) or HIV infection (n = 1). The HL in all 4 of these
patients was positive for EBV, also consistent with immunodeficiency. However, 18 patients in this study had no clinical evidence of immunodeficiency, and 8 (57%) of 14 cases assessed in
this apparently immunocompetent group also were positive for
EBV. This frequency is higher than the frequency of EBV in
most types of HL involving lymph nodes in immunocompetent
patients. Previous studies have reported that EBV can be detected in approximately 20% to 60% of classical HL, depending on
the histologic type, being lowest in nodular sclerosis and higher
in mixed cellularity.26 Because oropharyngeal epithelium is a
lifetime reservoir for EBV and many malignant neoplasms arising at this site are positive for EBV,2,3,14,17,18 it seems likely that
anatomic location rather than histologic type explains the higher
frequency of EBV in HL involving Waldeyer ring. OGrady and
colleagues27 made a similar suggestion based on the results of
their study in which they showed a higher frequency of EBV in

localized HL cases involving neck lymph nodes compared with

HL cases involving nonneck body sites. Because EBV LMP is
known to have oncogenic potential,28 it seems possible that EBV
has a role in pathogenesis rather than simply being a bystander.
In agreement with the literature, in the present study, HL
involving Waldeyer ring occurred most often in male patients
(16/22 [73%]) with local symptoms, and 18 (95%) of 19
patients whose disease was staged had stage I or II disease.3,14,16,20,21 Three patients had a history of NHL and were
not staged; 2 cases in this group were unusual because they had
concurrent evidence or a history of CLL/SLL. Thus, these cases
can be considered examples of the Hodgkin variant of Richter
syndrome. The term Richter syndrome is applied to the development of a secondary aggressive lymphoid malignancy in a
patient with a history of CLL/SLL.29 HL represents almost 15%
of all cases of Richter syndrome and occurs in approximately
1% of patients with CLL.30 Such cases have been referred to as
Richter syndrome with HL features or the Hodgkin type or variant of Richter syndrome. The literature recognizes 2 types of the
Hodgkin variant of Richter syndrome: type 1 is characterized by
Reed-Sternberg and Hodgkin cells scattered in a background of
CLL/SLL cells; in type 2, Reed-Sternberg and Hodgkin cells
are present within a polymorphous inflammatory tissue.31 Both
cases in the present study were type 2. Richter syndrome has
been associated with EBV infection.32,33 Although we are not
aware of other reported cases of Hodgkin-variant Richter syndrome involving Waldeyer ring, the high frequency of EBV at
this anatomic site may contribute to onset of this type of Richter
syndrome in these patients.
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Image 1 E, Hodgkin lymphoma associated with chronic lymphocytic leukemia/small lymphocytic lymphoma (CLL/SLL)
(Hodgkin-variant Richter syndrome); type II morphologic features with Hodgkin cells in a polymorphous inflammatory
background. The small lymphocytes expressed CD20 and CD5, characteristic of CLL/SLL (H&E, 400). F, The Hodgkin cells in
this case were positive for Epstein-Barr virus latent membrane protein-1(200).

Quiones-Avila et al / HODGKIN LYMPHOMA INVOLVING WALDEYER RING

In summary, HL involving Waldeyer ring is rare; we identified only 22 cases during 31 years. At our institution, the
lymphocyte-rich classical and nodular sclerosis types are most
common at this anatomic site, with the lymphocyte-rich classical type also predominating (4/7 [57%]) in patients with
stage I disease. We suggest that a subset of cases previously
described in the literature as mixed cellularity, nodular lymphocyte predominant, and unclassified HL may, in fact, have
been cases of lymphocyte-rich classical HL.
From the Department of Hematopathology, The University of
Texas M.D. Anderson Cancer Center, Houston.
Address reprint requests to Dr Medeiros: Dept of
Hematopathology, Box 72, UT M.D. Anderson Cancer Center,
1515 Holcombe Blvd, Houston, TX 77030.

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