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The objective of the study was to determine the frequency and pattern of Non Hodgkin's lymphoma (NHL) in adults in a tertiary care hospital. This retrospective study was conducted at Histopathology Department, Dr. Ziauddin Hospital over a period of 09 years, from 2003 to 2011. 192 cases of Non Hodgkin's lymphoma (NHL) were retrieved from surgical pathology record. After routine H and E stain examination, a panel of immunohistochemical stains was applied on formalin fixed paraffin embedded tissue. The data was analyzed for type of lymphoma, age and sex distribution, site of biopsy and immunophenotypic features. Out of 192 cases of Non Hodgkin's lymphoma (NHL), 132 (69%) were males and 60 (31%) were females. Mean age of patients was 46.7 years and median age was 47 years. B cell lymphoma was out numbered (87%) than T cell lymphoma (13%).

Diffuse large B-Cell lymphoma was the commonest (113) B cell lymphoma followed by other types of lymphoma. 52% cases were from extra nodal sites followed by 34% of nodal lymphoma. Site of biopsy was not mentioned in 14% cases.

In adults, B cell Lymphoma is more frequent than T cell Lymphoma with Diffuse large B-cell lymphoma being the commonest Non Hodgkin's Lymphoma.

Key Words: Lymphoma, Non Hodgkin's Lymphoma. Diffuse large B cell Lymphoma.


Lymphoma represents one of the major health problems all over the world. The Incidence of lymphoma is increasing largely contributed by Non Hodgkin's lymphoma (NHL). The age specific rates show a gradual rise from childhood to a gradual accent in the 7th decade. NHLs are slightly more common in developed countries (50.5% of cases worldwide), with rates highest in Australia and North America, intermediate inEurope(exceptEasternEurope)andthePacificislands, and relatively low throughout Asia and Eastern Europe.

In Asia, the incidence of non-Hodgkin lymphoma (NHL) has increased in recent decades.2 At national level, NHL is 4th most common malignancy in males accounting for 6.1%.3 Mortality and incidence rates from NHLs have also been reported to increase in both sexes in most countries over recent decades.

Diffuse large B cell lymphoma is the commonest NHL in the world.5 Alizadeh et al6 recently proposed a two-gene model based on the expression of a tumor biomarker LMO2 and a tumor microenvironment marker TNFRSF9 in patients with DLBCL. The twogene model was an independent predictor of survival in the multivariate analysis.

Patients with primary or secondary immunodeficiencies are at greater risk for lymphoma. These patients often show diffuse NHL morphologies, extranodal disease, and association with Epstein Barr virus (EBV) infection. Various occupational,environmental, and chemical agents have also been analyzed as risk factors for NHL.

Advances in immunophenotyping and improvement in the classification of haematological malignancies rendered better epidemiological comparison in the incidence and pattern of lymphoma.8 Deficient local data regarding lymphoma is available, hence clinical insight is needed to identify the exact picture of lymphoma. This study was conducted to see the frequency and pattern of Non Hodgkin's lymphoma in our setup.


This retrospective study was conducted at Histopathology Department of Dr Ziauddin Hospital, Karachi. 192 cases of Non Hodgkin's lymphoma were retrieved from surgical pathology records over a period of 09 years, from 2003 to 2011. After routine Hematoxyline and Eosine (HandE) stain examination, a panel of immunohistochemical stains was applied on formalin fixed paraffin embedded tissue.

The panel of lymphoid antibodies included: TdT, CD34, CD45, CD19,CD20, CD79, MUM-1 CDI0 ,CD21, CD23, CD3 ,CD4, CD5, CD8, CD15, CD30, CD43, CD56,CD68, MPO, Ki-67, Bcl-2, Bcl-6, Cyclin D1, Kappa, Lamda, ALK-1, ZAP 17 were used. Appropriate controls were placed on the same slide for each antibody, parallel to the patient's sections. The results were reported only after assuring that the controls have worked appropriately. The data was analyzed for type of lymphoma, age and sex distribution, site of biopsy and immunophenotypic features.


Out of 192 cases of Non Hodgkin's Lymphoma (NHL) 132 (69%) patients were males followed by 60 (31%) females. The male to female ratio was 2.2:1. Mean age of all NHL patients was 46.7 years with median being 47 years. Large number of patients diagnosed in 5th and 6th decade of life (Table 1) According to immuno-phenotypic profile 167 (87 %) cases of NHL were B cell phenotype and 25 (13%) cases were showed T cell/ NK cell phenotype. (Table 2)


Pakistan is a part of the lymphoma belt', the geographical boundaries of which extend from south-western Asia to Middle East to Northern Africa.9

Non Hodgkin's Lymphoma (NHL) is a broad category consisting of several distinct lymphoid neoplasms, presently classified according to universally accepted WHO classification, where many B and T cell subtypes are recognized.10

The current study showed a high number of cases of lymphoma were diagnosed in males (69%) than females (31%) These results are in agreement with findings by Haddadin WJ,11 Lee MY,12 Castella A et al13 and Hingorjo MR14 who also reported same results.


Age groups###No. of cases###% Percentage

###18-20 years###29###15

###21-30 years###29###15

###31-40 years###27###14

###41-50 years###39###20.3

###51-60 years###39###20.3

###61-70 years###15###8

###71- 80 years###14###7



Types###No. of###Percent-


B-Cell Phenotype (CD20 Pos-###167###87%


Diffuse large B cell Lymphoma###113###68

(CD20 Positive)

Small Lymphocytic lymphoma###17###10

(CD23 Positive)

Follicular lymphoma (CD10###10###06


T-cell rich large B cell Lym-###08###5

phoma (CD20 Positive)

Nodal marginal zone lym-###06###3.5


Mantle cell lymphoma (Cyclin###05###3

D1 Positive)

Maltoma (CD43 Positive)###04###2

Precursor B cell acute lympho-###03###2

lastic lymphoma

Primary cutaneous follicle###01###0.5

centre lymphoma

T-Cell / NK Cell Phenotype###25###13%

(CD3 Positive)


ALCL (CD 30 Positive)###07###28

Pre T ALL (TdT Positive)###03###12

Natural Killer Cell Lymphoma###02###8%

(CD56 Positive)

Grand Total###192###100


Sites Of biopsy###Number Percentage

###of cases

Lymph nodes###65###34

Extranodal NHL###99###52


Head and Neck###26

Reproductive Organs###10



Urinary system###4




No Site Stated###28###14

In present series an early presentation of NHL was seen in patients with mean age of 46.7 years. Other local studies15,16 also reported similar findings as mean age of 41.3 and 48.2 years. However these findings are not in agreement as compared to late presentation of 53.1 years reported by Kilickap S et al17 and other developed countries (56.4 years).18,19 It may be due to younger population, shorter life span, ethnic variations or other unknown reasons.

A study was done in Kualampur 20 also reported patients mean age as 42.1 years. The highest preponderance was in the age group of 51 to 60 years old, (20 cases, 22.0%), which is in agreement with findings of this study as large number of patients were in 5th and 6th decades. Reasons for an increased NHL risk with increasing aging have been attributed to decreasing immune function and a possibly higher susceptibility to infection, which in turn may render them more susceptible to many cancers including NHLs.21

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. Primary extranodal disease appears to be more common in Asia than the United States.7 NHL frequently has extranodal involvement and there are geographical differences in the incidence of extranodal NHL.22

The present study reported a large no. of lymphomas 99 (52%) were from extranodal sites as compared to (34%) lymph node involvement. These findings are in accordance with study done in Korea23 who also reported 69.6% cases of extranodal lymphoma than 30.4% cases of nodal lymphomas. However the results of current study are not in accordance to Mushtaq et al24 who found an increased number (62%) of nodal lymphomas than (38%) extranodal lymphoma. GI tract was found the commonest site of extranodal lymphoma in his study, which is similar with results of this study. 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.25

The distribution of NHL subtypes, however, revealed both similarities and some differences when compared with other NHL series from different Asian countries. In concordance with the majority of Asian studies, the proportion of low-grade lymphomas was small.13 The frequency of B and T cell NHL was same as observed in the previous Pakistani studies In current study an increased number of cases of NHL were showed B-cell phenotype 167 (87%) than T-cell 25 (13%). These results are in accordance to multiple international studies in Korea (B 78% / T 22%),23 Turkey (B 78% / T 16%)26 and Taiwan (B 87% / T 13%)12 and local studies by Naz E et al15 (B 85.5% / T 14.5%) and Mushtaq S et al24 (B 86% / T 14%) who also reported an increased B cell phenotype with variable frequency.

In Pakistan, though T cell lymphomas have been reported15,27,28 more as compared to western studies but overall T cell lymphomas are less frequent all over the world except the Far East Asian countries for unknown reasons. Nevertheless recognizing and diagnosing various subtype of T cell lymphomas according to WHO classification gives vital prognostic information. As generally the prognosis of T cell lymphomas is poorer than B cell Lymphomas.

Amongst the B cell Lymphomas, Diffuse large B cell Lymphoma is the commonest malignant lymphoma all over the world2,11,15,24,26 and the same was observed in the present series. The next commonest B cell lymphoma in present series was Small lymphocytic lymphoma followed by Follicular lymphoma. These results are not in agreement with other local studies.15,24 who reported Follicular lymphoma as 2nd commonest B cell lymphoma followed by Small lymphocytic lymphoma. Peripheral T cell Lymphoma-unspecified was common T cell Lymphoma in this study which was in accordance to a local study at AFIP and international studies done in Taiwan and Korea.

The lymphomas encompass an array of heterogeneous malignancies. Deficient local data is available, hence clinical insight is needed to identify the exact picture of NHL for further prevention, control and disease etiology, especially in terms of efficacy of treatment protocols being followed.

In conclusion, the relative frequency of malignant lymphoma in Karachi was not significantly changed and shows similarities with a previous nationwide study performed. Nevertheless, there were slight differences in the relative frequency of some subtypes, which may be caused by refined diagnostic criteria or a change of national healthcare policy. A population based epidemiologic study would be helpful to determine the true incidence of malignant lymphoma subtypes.


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Author:Bukhari, Uzma; Jamal, Saba; Lateef, Fouzia
Publication:Pakistan Oral and Dental Journal
Article Type:Report
Date:Sep 30, 2015

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