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1197
Malignant Lymphoma in Thailand
Changes in the Frequency of Malignant Lymphoma Determined from a
Histopathologic and Immunophenotypic Analysis of 425 Cases at Siriraj Hospital
Sanya Sukpanichnant, M.D.1
Dhira Sonakul, M.B., B.Ch., DMT&H1
Anong Piankijagum, M.D., Ph.D.2
Wanchai Wanachiwanawin, M.D., B.Sc.2
Gavivann Veerakul, M.D.3
Chularatana Mahasandana, M.D.3
Voravarn S. Tanphaichitr, M.D., M.S.3
Vinai Suvatte, M.D., Ph.D.3
1
Department of Pathology, Faculty of Medicine
Siriraj Hospital, Mahidol University, Bangkok, Thailand.
2
Department of Medicine, Faculty of Medicine
Siriraj Hospital, Mahidol University, Bangkok, Thailand.
3
Department of Pediatrics, Faculty of Medicine
Siriraj Hospital, Mahidol University, Bangkok, Thailand.
Presented in part at the 8th Meeting of the European Association for Haematopathology, La Villette-Paris, France, April 22–25, 1996.
Supported by Siriraj-China Medical Board Fund
Grant No. 75-348-213.
The authors thank Miss Kanittar Srisook for her
expertise in paraffin section immunoperoxidase.
Address for reprints: Sanya Sukpanichnant, M.D.,
Department of Pathology, Faculty of Medicine
Siriraj Hospital, Mahidol University, Bangkok
10700, Thailand.
Received November 17, 1997; revision received
March 20, 1998; accepted March 20, 1998.
© 1998 American Cancer Society
BACKGROUND. Analysis of malignant lymphoma in a single institution at different
periods of time can determine the changing status of the disease in the region.
METHODS. To compare with the large series of 1095 lymphoma cases reported
between 1957–1971 at Siriraj Hospital, the largest hospital in Thailand, a similar
study was performed through histopathologic evaluation of 425 lymphoma cases
diagnosed consecutively at the same institution between August 1993 and October
1995. Phenotypic analysis was performed by paraffin section-immunoperoxidase
studies.
RESULTS. A striking increase in lymphoma cases was noted from 73 cases/year in
the first series to 189 cases/year in the second series (an increase of 158.9%).
Lymphoma occurred in all age groups, with a peak incidence at the seventh decade
of life. The male to female ratio decreased from 2:1 in 1957–1971 to 1.3:1 in the
more recent series. The incidence of Hodgkin’s disease (HD) was found to have
decreased from 28.9% to 8.5%. There were 36 cases (8.5%) of HD and 389 cases
(91.5%) of non-Hodgkin’s lymphoma (NHL) reported in the second series. The
subtypes of HD included 16 cases of mixed cellularity, 13 cases of nodular sclerosis,
6 cases of lymphocyte depletion, and 1 case of lymphocyte predominance. According to the Working Formulation, the 389 NHL cases included low grade (14.1%),
intermediate grade (57.3%), high grade (11.3%), and miscellaneous groups (17.2%).
They were classified as small lymphocytic (9.5%), follicular (11.1%), diffuse (50.9%),
immunoblastic (4.1%), small noncleaved (4.4%), lymphoblastic (2.8%), anaplastic
large cell (9.0%), mycosis fungoides (1.8%), hairy cell leukemia (0.3%), true histiocytic (0.5%), and extramedullary plasmacytoma (1.0%). The immunophenotypes
of the 359 NHL cases available for paraffin section-immunoperoxidase studies
were B-cell (71.0%), T-cell (24.5%), histiocyte (0.6%), and undetermined phenotypes (3.9%).
CONCLUSIONS. The incidence of malignant lymphoma is increasing in Thailand,
with a high frequency of intermediate to high grade NHL of B-cell phenotype
reported. Cancer 1998;83:1197–204. © 1998 American Cancer Society.
KEYWORDS: lymphoma, Hodgkin’s disease, non-Hodgkin’s lymphoma, Thailand,
classification, immunophenotype, extranodal lymphoma, childhood lymphoma.
I
n 1980, Piankijagum et al. from Siriraj Hospital, Bangkok, Thailand,
reported a series of 1,095 cases of malignant lymphoma.1 This series
has been regarded as the largest series of lymphoma cases ever
published from a single institution in Thailand. The data were based
on biopsied materials received in the Department of Pathology at
Siriraj Hospital during a 15-year period (1957–1971). The patients
originated from all four regions of the country: central, north, northeast, and south. Of the total 140,323 specimens acquired during the
study period, 1095 cases of malignant lymphoma were identified. The
1198
CANCER September 15, 1998 / Volume 83 / Number 6
histologic types of malignant lymphoma in that series
were classified as Hodgkin’s disease (HD) (316 cases,
28.9%); reticulum cell sarcoma (472 cases; 43.1%);
lymphosarcoma, including lymphocytic and lymphoblastic lymphoma (229 cases; 20.9%); giant follicular
lymphoma (20 cases; 1.8%); Burkitt’s lymphoma (1
case; 0.1%); and unclassified lymphoma (57 cases;
5.2%) according to the criteria used by Thai pathologists during that period,2 which was prior to the publication regarding tumors of the hemopoietic system
by Rappaport in 1966.3 The relative incidence of malignant lymphoma in different regions of Thailand
followed the same pattern as the overall incidence.
Male preponderance was shown with male to female
ratio for non-Hodgkin’s lymphoma (NHL) ranging
from 2.1:1 to 2.7:1 and was very striking for HD occurring in childhood (5.7:1). The mean age for HD was
35.4 years, whereas the mean ages for reticulum cell
sarcoma and lymphosarcoma were 41.8 years and 40.5
years, respectively.
Malignant lymphoma between 1957–1971 was
considered uncommon at Siriraj Hospital (approximately 73 cases reported per year). However, hematologic malignancies, including malignant lymphoma
and leukemia, currently are ranked as the second most
common cancer at Siriraj Hospital,4 which is the largest hospital in Thailand with 2400 inpatient beds. The
hospital also is regarded as the largest referral center
for hematologic diseases in Thailand. Patients from all
regions of the country have access to the hospital,
which is a government-based hospital and one of the
best known medical schools in Thailand. Due to the
better understanding and more precise diagnosis of
malignant lymphoma by histologic approach in conjunction with immunophenotypic studies, we believed
it would be interesting to determine whether the status of malignant lymphoma has been changing since
the first series of malignant lymphomas was reported
from our institution by Piankijagum et al.1 The current
study was conducted to analyze cases of malignant
lymphoma by histopathologic and immunophenotypic means. Comparison with the recent study of
NHL in Thailand reported by Intragumtornchai et al.5
also was performed.
MATERIALS AND METHODS
Consecutive cases of lymphoma were collected at
Siriraj Hospital during the 27-month period between
August 1993 and October 1995 based on biopsied materials received at the Department of Pathology, similar to the approach used in the first series of malignant lymphoma reported from our institution.1
Malignant lymphoma was established in all cases by
histology in conjunction with immunophenotypic
studies by paraffin section-immunoperoxidase and
classified according to the Working Formulation (National Cancer Institute)6 for NHL and the Rye classification7 for HD. In all cases, the diagnosis was made in
consensus by two hematopathologists (S.S. and D.S.).
The Working Formulation was used in this study because it has been recommended among Thai pathologists since 1987 and is well accepted by Thai hematologists. Paraffin section-immunoperoxidase was the
only technique available in our institution for immunophenotyping malignant lymphoma; therefore, no
attempt was made to classify malignant lymphoma
according to the revised European–American classification of lymphoid neoplasms (Revised EuropeanAmerican classification of Lymphoid neoplasms
[R.E.A.L.] classification)8 due to incomplete data regarding the immunophenotypes, many of which required frozen-section-immunoperoxidase or flow cytometry.
Paraffin section-immunoperoxidase was performed using the labeled streptavidin-biotin-peroxidase method to characterize B-cell by CD20 (L-26),
T-cell by CD45RO (UCHL-1), CD43 (Leu22) or polyclonal CD3, histiocyte by CD68 (KP-1), Reed–Sternberg cells by CD15 (LeuM-1) and CD30 or Ki-1 (BerH2). Plasma cells were evaluated for immunoglobulins
G, A, and M, as well as k, and l light chains. Leukocyte
common antigen (LCA) (CD45), epithelial membrane
antigen (EMA), and cytokeratin also were included in
the study. In conjunction with the histologic evaluation of malignant lymphoma, the immunoperoxidase
stainings were evaluated to establish the phenotype in
each case as described in the standard hematopathologic textbooks.9 –13 Briefly stated, the neoplastic cells
in all subtypes of HD, with the exception of nodular
lymphocyte predominant subtype, showed immunoreactivity with CD15 and CD30 in the absence of immunoreactivity with LCA and EMA. The neoplastic
cells in nodular, lymphocyte-predominant HD
showed immunoreactivity of B-cell phenotype
(CD201, CD451) and were EMA positive (1) with
negative CD15 and CD30 stainings. The B-cell phenotype of NHL was established when the neoplastic cells
showed immunoreactivity with CD20 and CD45. They
may bear monoclonal immunoglobulin or have light
chain restriction. They were negative for T-cell and
histiocytic markers. The T-cell phenotype of NHL was
established when the neoplastic cells showed immunoreactivity with at least one of the three T-cell markers (CD45RO, CD43, and polyclonal CD3) and CD45
with negative CD20, immunoglobulins, CD68, and
CD15 stainings. The histiocytic phenotype of NHL was
established when the neoplastic cells showed immunoreactivity with CD68 in the absence of pan-B, pan-
Malignant Lymphoma in Thailand/Sukpanichnant et al.
1199
TABLE 1
Histologic Grades and Immunophenotypes of 389 Cases of Non-Hodgkin’s Lymphoma at Siriraj Hospital According to the Working Formulation
for Clinical Usage in NHL3
Histologic grade
No. of cases
B-cell
T-cell
Histiocytic
Undetermined
NA
Low
55
(14.1%)
223
(57.3%)
44
(11.3%)
67
(17.2%)
389
(100%)
36
(78.3%)
163
(77.6%)
27
(69.2%)
29
(45.3%)
255
(71.0%)
8
(17.4%)
41
(19.5%)
11
(28.2%)
28
(43.8%)
88
(24.5%)
—
2
(4.3%)
6
(2.9%)
1
(2.6%)
5
(7.8%)
14
(3.9%)
9
Intermediate
High
Miscellaneous
Total cases
—
—
2
(3.1%)
2
(0.6%)
13
5
3
30
NHL: non-Hodgkin’s lymphoma; NA: not available for paraffin section-immunoperoxidase.
T-cell markers, CD15, and CD30. Plasmacytoma
showed monoclonal immunoglobulin staining or light
chain restriction. CD30 could be positive in NHL
cases, especially NHL with anaplastic features; in such
cases the neoplastic cells showed a definite B- or T-cell
phenotype as described earlier. When a B- or T-cell
phenotype could not be demonstrated in some
CD301 NHL cases the histology in such cases was not
that of HD and immunoreactivity with CD45 in the
absence of cytokeratin was necessary.
RESULTS
Of the total 32,847 biopsied specimens acquired during the 27-month period, 425 consecutive cases of
malignant lymphoma were diagnosed (average, 189
cases per year): 36 cases of HD (8.5%) and 389 cases of
NHL (91.5%). The histologic subtypes of HD included
16 mixed cellularity (MCHD) (44.4%), 13 nodular sclerosis (NSHD) (36.1%), 6 lymphocyte depletion (16.7%),
and 1 lymphocyte predominance (2.8%). According to
the Working Formulation for clinical usage in NHL,
intermediate and high grade lymphomas constituted
the majority of NHL (68.6%) whereas low grade lymphoma comprised only 14.1% of all NHL (Table 1).
Both HD and NHL occurred in all age groups (Fig.
1). The mean age of HD patients was 27.1 years (range,
4 –70 years) whereas the mean age of NHL patients
was 47.1 years (range, 1–98 years). The age peak in HD
was in the third decade. Nine of 36 cases of HD (2
NSHD and 7 MCHD) were in children (age , 15 years).
The majority of NHL occurred between the third and
eighth decades with an age peak in the seventh decade. Intermediate grade NHL was the most common
in all age groups except for the first decade of life in
which high grade NHL was most common. Low grade
NHL occurred in the fourth decade and later. The
male to female ratio was 1.3:1 overall. We found no
FIGURE 1. Age distribution of the patients with malignant lymphoma at Siriraj
Hospital (1993–1995) demonstrated by histogram. Low, intermediate, and high
grades of non-Hodgkin’s lymphoma were classified according to the Working
Formulation of the National Cancer Institute.6 HD: Hodgkin’s disease; NHL:
non-Hodgkin’s lymphoma.
gender differences in adult HD (1.3:1) or low and
intermediate grade NHL (1.2:1 each), but there was
male preponderance in childhood HD (3.5:1), high
grade NHL (1.9:1), and anaplastic large cell lymphoma
(2.5:1).
There were 359 cases (92.3%) available for paraffin
section-immunoperoxidase studies. B-cell phenotype
was the most common type of NHL (71.0%); T-cell
phenotype comprised approximately one-fourth of all
NHL (24.5%). We found only 2 cases of true histiocytic
lymphoma (0.6%) and failed to demonstrate a phenotype in 3.9% of NHL (Table 1). Both B-cell and T-cell
NHL occurred in all age groups. The mean age in
B-cell NHL was 51.1 years (range, 2–98 years) whereas
that in T-cell NHL was 36.5 years (range, 1–91 years).
1200
CANCER September 15, 1998 / Volume 83 / Number 6
TABLE 2
Histologic Subtypes and Immunophenotypes of NHL According to the Working Formulation
Histologic type-no. of cases (%)
No. tested
B-cell (%)
T-cell (%)
Histiocyte (%)
U (%)
Small lymphocytic-37 (9.5%)
Follicular, small cell-11 (2.8%)
Follicular, mixed-7 (1.8%)
Follicular, large cell-25 (6.4%)
Diffuse, small cell-4 (1.0%)
Diffuse, mixed-88 (22.6%)
Diffuse, large cell-106 (27.2%)
Immunoblastic-16 (4.1%)
Small noncleaved-17 (4.4%)
Lymphoblastic-11 (2.8%)
True histiocytic-2 (0.5%)
Anaplastic large cell-35 (9.0%)
Hairy cell leukemia-1 (0.3%)
Plasmacytoma-4 (1.0%)
Mycosis fungoides-7 (1.8%)
Unclassifiable-18 (4.6%)
34
7
5
23
4
85
98
16
13
10
2
35
1
4
6
16
24 (70.6%)
7 (100%)
5 (100%)
23 (100%)
4 (100%)
52 (61.2%)
84 (85.7%)
15 (93.8%)
12 (92.3%)
—
—
15 (42.9%)
1 (100%)
4 (100%)
—
9 (56.3%)
8 (23.5%)
—
—
—
—
33 (38.8%)
8 (8.2%)
1 (6.3%)
—
10 (100%)
—
15 (42.9%)
—
—
6 (100%)
7 (43.8%)
—
—
—
—
—
—
—
—
—
—
2 (100%)
—
—
—
—
—
2 (5.9%)
—
—
—
—
—
6 (6.1%)
—
1 (7.7%)
—
—
5 (14.3%)
—
—
—
—
NHL: non-Hodgkin’s Lymphoma; U: undetermined phenotype.
The age peak in B-cell NHL was in the sixth decade.
The age distribution of T-cell NHL was bimodal with
one peak in the second decade and the other in the
seventh decade. No gender predilection was noted in
either B- or T-cell NHL (male:female 5 1.3:1 and 1:1,
respectively).
According to the subtypes of NHL in the Working
Formulation, diffuse, large cell type and diffuse, mixed
cell type were the two most common types (106 cases
[27.2%] and 88 cases [22.6%], respectively) (Table 2).
B-cell was the most common phenotype among these
two types of lymphomas (85.7% and 61.2%, respectively). In terms of histologic correlation with particular phenotypes of lymphomas in this series, follicular
lymphomas of all subtypes, when tested, were of B-cell
phenotype. Plasmacytoma was another B-cell neoplasm. Hairy cell leukemia, a rare condition in Thailand, was found to be of B-cell phenotype. However,
we encountered a case of T-cell small lymphocytic
lymphoma simulating hairy cell leukemia morphologically in the bone marrow section, but no circulating
cells with cytoplasmic projections were found. Nearly
all small noncleaved cell lymphomas in our series
were of B-cell phenotype (92.3%); in only 1 case (7.7%)
could the phenotype not be determined. The majority
of immunoblastic lymphomas were B-cell neoplasms
(93.8%). It is interesting to note that T-cell immunoblastic lymphoma does exist; one case was found in
our series. When tested in our series all lymphoblastic
lymphoma and mycosis fungoides (cutaneous T-cell
lymphoma) were of T-cell phenotype. We also identified a case of diffuse large B-cell lymphoma of the
paranasal sinus found to have epidermotropism by
lymphoma cells in the skin nodule, simulating mycosis fungoides, at the time of recurrence.
Based on tissue samples received at the Department of Pathology, Siriraj Hospital, we found that 214
of 389 cases of NHL (55.0%) had extranodal involvement by lymphoma (Table 3). The upper aerodigestive
tract and gastrointestinal (GI) tract were the two most
common extranodal sites of NHL (59 cases [15.2%]
and 33 cases [8.5%], respectively). Among the lymphomas involving the upper aerodigestive tract were low
grade (4 cases), intermediate grade (48 cases), high
grade (6 cases), and plasmacytoma (1 case). T-cell
lymphoma was predominant in the nasal passages (11
of 15 cases) and B-cell lymphoma was predominant in
the tonsil, oral cavity and palate, and nasopharynx
(Table 4). The mean age of the patients with lymphoma involving the upper aerodigestive tract was 51
years (range, 14 – 85 years). The male to female ratio
was 1.1:1.
Among the lymphomas involving the GI tract, 30
cases (91%) were primary GI lymphoma and the other
3 cases were comprised of GI involvement in advanced nodal lymphoma. The histologic subtypes of
GI lymphomas were low grade (9 cases), intermediate
grade (16 cases), and high grade (8 cases). Nearly all
were B-cell lymphoma when tested for immunophenotype (B-cell: 26 cases; T-cell: 1 case; and undetermined phenotype: 3 cases). Four of nine small lymphocytic lymphomas were characteristic of low grade
lymphoma of mucosa-associated lymphoid tissue, a
recently recognized lymphoma14; two additional cases
were suggestive of this specific lymphoma. The only
case of low grade T-cell lymphoma of the ileum was
Malignant Lymphoma in Thailand/Sukpanichnant et al.
1201
TABLE 3
The Immunophenotypes of NHL Involving Extranodal Sites Based on Tissue Samples Submitted for Pathologic Examination
Site of involvement
No. of cases
B-cell
T-cell
U
NA
Upper aerodigestive
Gastrointestinal
Skin
Soft tissue
Liver
Bone
Spleen
Brain
Lacrimal gland, eyelid, and conjunctiva
Pleura
Retroperitoneum
Mediastinum
Salivary gland
Subcutaneous tissue
Ovary
Testis
Orbit
Pelvic mass
Abdominal mass
Thyroid gland
Pancreas
Trachea
Breast
Extradural
Total
59
33
19
17
13
12
9
8
6
6
5
4
4
4
2
2
2
2
2
1
1
1
1
1
214
34
27
4
12
6
6
2
7
6
—
5
2
4
—
1
2
2
2
1
1
1
—
—
—
125
14
1
14
2
7
1
7
—
—
5
—
2
—
3
—
—
—
—
—
—
—
1
—
—
57
3
3
—
—
—
2
—
—
—
1
—
—
—
—
—
—
—
—
—
—
—
—
—
—
9
8
2
1
3
—
3
—
1
—
—
—
—
—
1
1
—
—
—
1
—
—
—
1
1
23
NHL: non-Hodgkin’s lymphoma; U: undetermined phenotype; NA: not available for paraffin section-immunoperoxidase.
TABLE 4
The Immunophenotypes of NHL Involving the Upper
Aerodigestive Tract
TABLE 5
Histologic and Immunophenotypic Findings in 40 Cases of
Childhood NHL
Site of involvement (no.)
B-cell
T-cell
U
NA
Histologic type (no. of cases)
B-cell
T-cell
U
NA
Nasal (15)
Nasopharynx (9)
Paranasal sinuses (5)
Tonsil (18)
Oral cavity and palate (8)
Tongue (4)
2
6
3
13
6
4
11
1
1
—
1
—
1
—
1
1
—
—
1
2
—
4
1
—
Small lymphocytic (4)
Large cell (15)
Small noncleaved cell (11)
Lymphoblastic (5)
Unclassifiable (5)
Total cases (40)
—
4
7
—
2
13
(36.1%)
3
10
—
4
3
20
(55.6%)
1
1
1
—
—
3
(8.3%)
—
—
3
1
—
4
NHL: non-Hodgkin;s lymphoma; U: undetermined phenotype; NA: not available for paraffin sectionimmunoperoxidase.
enteropathy-associated, T-cell lymphoma, another recently described entity.14 This patient had chronic
diarrhea and was misdiagnosed by other hospitals as
having immunoproliferative small intestinal disease
for years. The mean age of the patients with lymphoma involving the GI tract was 45.3 years (range,
2– 81 years). The male to female ratio was 2.3:1.
Childhood NHL constituted 10.3% of all NHL in
our series because only 40 patients were age , 15
years. The histologic types according to the Working
Formulation and the phenotypes of childhood NHL
NHL: non-Hodgkin’s lymphoma; U: undetermined phenotype; NA: not available for paraffin sectionimmunoperoxidase.
are demonstrated in Table 5. Practically, childhood
NHL mainly includes lymphoblastic, small noncleaved cell, and large cell lymphomas.15 Therefore,
large cell lymphoma constituted 37.5% of all childhood NHL when diffuse lymphoma and anaplastic
large cell lymphoma were included. Small noncleaved
cell lymphoma was the second most common (27.5%)
and lymphoblastic lymphoma constituted 12.5% of all
childhood NHLs. T-cell lymphomas were more prevalent in childhood (55.6%) when compared with the
1202
CANCER September 15, 1998 / Volume 83 / Number 6
TABLE 6
The Changing Status of Malignant Lymphoma at Siriraj Hospital:
Comparison between the Series Reported by Piankijagum et al.1 and
the Current Study
Period of study
No. of patients
Average no. of cases/yr
Age peak incidence
Male:female
NHL/HD (%)
Piankijagum et al.
The current study
15 years (1957–1971)
1095
73
6th decade
2:1
71.1/28.9
27 months (1993–1995)
425
189
7th decade
1.3:1
91.5/8.5
NHL: non-Hodgkin’s lymphoma; HD: Hodgkin’s disease.
frequency of T-cell lymphoma in the overall cases of
NHL (24.5%).
Only 5 cases of acquired immunodeficiency syndrome (AIDS)-associated lymphoma could be documented. All these patients were male, ranging in age
from 21–27 years. Three of these patients had lymph
node enlargement that was proven to be small noncleaved cell lymphoma; two of these patients had a
B-cell phenotype when tested. Another patient had
lymph node enlargement that was proven to be a high
grade lymphoma of unclassifiable type due to extensive necrosis; however, B-cell phenotype was established in this case. The fifth patient had advanced
disease presenting with a tibial lesion proven to be
anaplastic large cell lymphoma of T-cell phenotype.
DISCUSSION
To our knowledge, the current series of malignant
lymphoma is the largest one in Thailand to study both
histology and immunophenotypes of NHL. When
compared with the first series from our institution
conducted between 1957–1971,1 the rising number of
cases of malignant lymphoma was striking (Table 6),
from 73 cases per year to 189 cases per year (an increase of 158.9%), whereas the number of biopsied
specimens increased from 9355 specimens per year to
14,599 specimens per year (56.1%). We believe that
there are several reasons for this changing status in
malignant lymphoma. First, histologic evaluation in
conjunction with immunophenotypic studies plays an
important role in the diagnosis of malignant lymphoma in several cases that might have been diagnosed as undifferentiated neoplasm, carcinoma, or
even sarcoma in the past based on histology alone.
Second, there are more hematologists to recognize
more cases of malignant lymphoma. At the time of the
first series from our institution, there were only 2
centers for hematologic diseases and approximately
15 hematologists throughout the country. To date,
there are 14 centers (8 of which are in medical schools:
5 in the central region and 1 each in the north, northeast, and south) and 105 registered hematologists
(data provided by the Society of Hematology of Thailand in 1996). Third, the improved standard of the
health care system in Thailand provides easier patient
access to the hospitals. Nevertheless, we believe that
the incidence of malignant lymphoma in Thailand is
increasing when we combine the number of adult
NHL from the series recently reported by Intragumtornchai et al.5 (278 cases per year) with the number of
malignant lymphomas in the current series (189 cases
per year) (at least 467 cases of malignant lymphoma
that are newly diagnosed per year in Thailand). A
tumor registry of malignant lymphoma and a nationwide epidemiologic study are needed to confirm the
increasing incidence of malignant lymphoma. Moreover, the incidence of HD has decreased significantly.
We believe the main reason for such a change is the
better characterization of lymphoma with the help of
immunohistochemistry.
Intragumtornchai et al.5 recently reported a large
series of 1391 cases of adult NHL (age $ 15 years) in
Thailand from a compilation of cases diagnosed in 6
medical centers during a 5-year period (1988 –1992)
from 4 different regions of the country (central [3
centers; 554 cases], north [1 center; 391 cases], northeast [1 center; 223 cases], and south [1 center; 223
cases]) varying from 20 –78 cases per year in these 6
medical centers. The histologic types of NHL in each
center were not reviewed by the panel of pathologists
for a consensus diagnosis; however, the authors concluded that the frequencies of the pathologic subtypes
reported from each center followed a similar pattern.
Only 130 of the total 1391 cases (9.3%) were immunophenotyped in their series. Nevertheless, our results
agree with their series and other series in Asia that
show that low grade lymphoma is less common in Asia
than in the U.S. whereas intermediate to high grade
lymphomas are more common in Asia than in the
U.S.16 This remains true when we examine adult NHL
in our series. Of the 349 cases, there were 51 cases of
low grade (14.6%), 212 cases of intermediate grade
(60.7%), 28 cases of high grade (8.0%), and 58 cases of
miscellaneous group including anaplastic large cell
lymphoma (ALCL) (16.6%). The immunophenotypes
of NHL from our series confirms those from the series
reported by Intragumtornchai et al.5 (Table 7). This
relative frequency is similar to that published in the
standard textbooks from the U.S. and Europe.9 –13
When the relative frequency of B-cell and T-cell lymphoma is compared with that reported in Taiwan,
China, Hong Kong, and Japan, there is less T-cell lymphoma in Thailand.16 Human T-cell lymphoma virus-
Malignant Lymphoma in Thailand/Sukpanichnant et al.
TABLE 7
Comparison of the Immunophenotype in NHL with Histologic
Correlation between the Current Study at Siriraj Hospital and the
Series Reported by Intragumtornchai et al.5
Immunophenotype and
histologic grade
The current study
(359 cases)
Intragumtornchai et al.
(130 cases)
B-cell
Low grade
Intermediate grade
High grade
Miscellaneous
T-cell
Low grade
Intermediate grade
High grade
Miscellaneous
Histiocytic
Undetermined
phenotype
255 (71.0%)
36 (10.0%)
163 (45.4%)
27 (7.5%)
29 (8.1%)
88 (24.5%)
8 (2.2%)
41 (11.4%)
11 (3.1%)
28 (7.8%)
2 (0.6%)
100 (76.9%)
14 (10.8%)
78 (60.0%)
6 (4.6%)
2 (1.5%)
21 (16.2%)
—
11 (8.5%)
3 (2.3%)
7 (5.4%)
—
14 (3.9%)
9 (6.9%)
type 1 may be associated with the higher frequency of
T-cell lymphoma in Japan and Taiwan.17 To the best of
our knowledge, adult T-cell leukemia/lymphoma has
not been reported in Thailand.
The incidence of follicular lymphoma in our series
was low (43 cases; 11.1%) when compared with that
encountered in the U.S.9 However, the frequency of
follicular lymphoma in our series was higher than that
reported by Intragumtornchai et al. (3.8%). Interpathologist agreement and intrapathologist reproducibility in making a histologic diagnosis of follicular
lymphoma are well recognized.18 In Thailand, to our
knowledge no study has addressed such reproducibility in diagnosing follicular lymphoma. In our experience, we have encountered a number of cases of follicular lymphoma with a vaguely follicular or nodular
appearance that were misdiagnosed as diffuse lymphoma by outside pathologists. However, these cases
demonstrated a more distinctly follicular appearance
at the time of recut for better histologic sections or
subsequent biopsies. The frequency of small lymphocytic lymphoma in our series (9.5%) was comparable
to that of Intragumtornchai et al. (10%).
We have previously confirmed the usefulness of
histologic recognition for certain types of NHL to predict the immunophenotypes of lymphoma, including
follicular lymphoma (B-cell), plasmacytoma (B-cell),
small noncleaved cell lymphoma (B-cell), lymphoblastic lymphoma (T-cell), and mycosis fungoides or cutaneous T-cell lymphoma (T-cell).9 –13 However, we
should emphasize that at times distinguishing between various types of NHL is not possible even in
cases with appropriate fixation of the specimens and
high quality histologic sections. In this situation, mul-
1203
tiparameter analysis to establish a definite diagnosis
includes immunophenotyping by paraffin section- or
frozen section-immunoperoxidase or by flow cytometry, electron microscopy, cytogenetic study, and molecular genetic study.9 –13
ALCL in our series was diagnosed by the anaplastic features of the lymphoma cells, the sinus distribution, and the immunoreactivity with CD30.19 We
found that ALCL was of either B-cell or T-cell phenotype equally (42.9%) and 14.3% were of undetermined
phenotype. No attempt was made to follow the
R.E.A.L. classification that placed ALCL of B-cell phenotype into the diffuse large B-cell lymphoma category.8
The common extranodal involvement in NHL is
well documented in the literature9 –13 and confirmed
in our series (55.0%). Lymphoma can occur in any
organ or tissue due to the ubiquity of hematopoietic
lymphoid system; therefore, lymphoma often is included in the differential diagnosis of neoplasm.
Awareness of the possible existence of extranodal lymphoma correctly should lead to a rapid diagnosis. This
fact should be recognized by physicians who are not
hematologists or oncologists.
It is interesting to examine why certain types of
lymphomas tend to have one particular immunophenotype. The higher frequency of T-cell lymphoma in
childhood is another interesting issue. Because malignant lymphoma is comprised of many different types
with regard to biologic and clinical behavior, it will be
very useful to determine which particular groups of
lymphomas that can be cured, controlled, or even
prevented. For instance, the Epstein–Barr virus (EBV)
is among a number of etiologic agents proposed in
lymphomagenesis.20 Recently, EBV genomes were
demonstrated in most nasal T-cell/natural killer cell
lymphomas.21 One case of nasal T-cell lymphoma in
our series was included in that article via a T-cell
lymphoma workshop organized in Hong Kong in 1995;
in this case EBV genomes were demonstrated by in
situ hybridization.21 EBV genomes have been found in
many types of malignant lymphoma of either B-cell or
T-cell phenotype.20
Despite the high rate of human immunodeficiency virus infection in Thailand, only 5 cases of
documented AIDS-associated lymphoma were noted
in this series (5 of 389 NHL; 1.3%). Similarly, Kaposi’s
sarcoma is not common in AIDS patients in Thailand.22 The underlying reason for this unique feature
of AIDS-related neoplasms in Thailand is not known
and further investigation is needed.
The current study emphasizes the significance of
lymphoma especially of NHL. The significant increase
in the number of cases of NHL encountered at Siriraj
1204
CANCER September 15, 1998 / Volume 83 / Number 6
Hospital requires further study regarding epidemiology and lymphomagenesis.
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