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Indian Journal of Medical and Paediatric Oncology
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Year : 2018  |  Volume : 39  |  Issue : 1  |  Page : 42-45  

Non-Hodgkin's lymphoma in Northern India: An analysis of clinical features of 241 cases

Department of Medical Oncology, Institute Rotary Cancer Hospital, All India Institute of Medical Sciences, New Delhi, India

Date of Web Publication29-Jan-2018

Correspondence Address:
Dr. Devinder Singh Sandhu
Sandhu Cancer Centre, Udham Singh Nagar Market, Civil Lines, Ludhiana - 141 001, Punjab
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmpo.ijmpo_36_17

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Background: Geographic variations with regard to incidence, clinical presentation, and histological subtypes are known to occur in several cancers. This study was aimed to see if similar differences existed in non-Hodgkin's lymphoma (NHL) also during pre-immunohistochemical era. Materials and Methods: Cases of NHL seen at Institute Rotary Cancer Hospital, All India Institute of Medical Sciences, New Delhi from January 1997 to December 2000, were analyzed for baseline clinical features and histology. Results: Total cases: 241, median age: 47 years (range 2–84 years), male-female ratio: 2.2:1, primary extranodal NHL: 44.2%, the most common histological subtype: Diffuse large cell (6.2% of the cases). Conclusion: Our patients presented at younger median age, had more male to female ratio, had diffuse large cell histology as the most common histological subtype.

Keywords: Extranodal non-Hodgkin's lymphoma, non-Hodgkin's lymphoma, Northern India

How to cite this article:
Sandhu DS, Sharma A, Kumar L. Non-Hodgkin's lymphoma in Northern India: An analysis of clinical features of 241 cases. Indian J Med Paediatr Oncol 2018;39:42-5

How to cite this URL:
Sandhu DS, Sharma A, Kumar L. Non-Hodgkin's lymphoma in Northern India: An analysis of clinical features of 241 cases. Indian J Med Paediatr Oncol [serial online] 2018 [cited 2021 Jan 28];39:42-5. Available from: https://www.ijmpo.org/text.asp?2018/39/1/42/224025

  Introduction Top

The incidence of non-Hodgkin's lymphoma (NHL) is rising worldwide. In addition, geographic variations in its incidence and clinical behavior are well known.[1] NHL despite being the most common lympho-hematopoietic malignancy in India, has lower age-standardized incidence rate (ASR) (0.8–5.1 males, 0.6–3.1 females) than that seen in the USA (16.1 males and 10.8 females). Low-grade NHL (follicular lymphoma, and chronic lymphocytic leukemia) is more common in the USA, whereas diffuse large B cell lymphoma is more common in India, Burkitt's lymphoma occurs more frequently in tropical Africa, Immunoproliferative small intestinal disease in the Middle East and adult T-cell leukemia/lymphoma in South West Japan and the Caribbean basin.[1],[2],[3],[4] Despite being a large country publications for NHL from India in general and northern India, in particular, are limited. The subclassification of NHL has gone substantial changes with the availability of new immunohistochemical markers, and also the availability of monoclonal antibody (anti-CD 20 antibody) has changed the treatment outcome of B-cell lymphoma,[1] but this study predates these or when these parameters or treatment options were not freely available to our patients and diagnosis was based mainly on morphology. Hence, we decided to analyze the clinical features of NHL seen at our center.

  Materials and Methods Top

Patients of NHL registered at Institute Rotary Cancer Hospital (IRCH), All India Institute of Medical Sciences (AIIMS) between January 1, 1997 and December 31, 2000 were included in this study. The IRCH files of the patients were taken from the record section and scrutinized for the epidemiological, clinical, and laboratory data. Confirmation of the histopathological diagnosis at AIIMS was mandatory for inclusion in the study. Other inclusion criteria were treatment naive and those who received treatment at AIIMS. Patients with fine-needle aspiration cytology based diagnosis were excluded.

Working formulation classification of NHL was used for classification.[4] Ann Arbor classification was used to staging the patients.[5] The stage at initial presentation was determined on the basis of clinical, radiological, and laboratory data available in the files.

  Results Top

Of the 241 patients included in the study, 168 were male and 73 were female with a male to female ratio of 2.2:1. The median age at presentation was 47 years, range 2–84 years. “B” symptoms were present in 104 patients (43.2%).

One hundred and sixty-seven patients (69.3%) had peripheral lymphadenopathy, whereas 107 (44.4%) had axial lymphadenopathy [Table 1]. It was generalized (involvement of 3 or more noncontiguous lymph node areas) in 54 cases (22.4%). Individual sites of lymphadenopathy are shown in [Table 1]. Bulky lymphadenopathy was seen in 41 patients (17%) and superior vena cava syndrome in 4 (1.7%) at presentation.
Table 1: Clinical presentation of 241 cases

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Primary extranodal NHL (when the extra nodal site is the only site of disease, or the bulk of disease is confined to extranodal sites)[6] was seen in 106 cases (44.2%). Head and neck region was the most common region (53 cases - 22%) of extranodal involvement followed by gastrointestinal tract (GIT) (29 cases - 12%). Various sites and sub sites of extranodal disease are shown in [Table 2].
Table 2: Primary extra nodal NHL, 106 cases (44.2%)

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The diffuse large cell was the most common histological subtype based on Working Formulation classification [Table 3]. It accounted for 146 cases (60.58%). Other subtypes included follicular small cleaved cell – 15 (6.2%) cases, diffuse small cleaved cell – 11 (4.6%), diffuse mixed cell – 11 (4.6%), lymphoblastic – 9 (3.7%), follicular mixed cell – 5 (2.1%), large cell immunoblastic – 3 (1.2%), small noncleaved cell – 3 (1.2%), and follicular large cell – 1 (0.4%). Unspecified and other histologies accounted for 31 cases.
Table 3: Histological subtypes, working formulation based

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More than 50% of the patients had advanced Stage of III and IV at presentation, Stage III – 45 cases (18.4%), and Stage IV – 84 cases (35.1%) [Table 4]. Early stage was seen in 112 cases, Stage I – 55 cases (22.8%), and Stage II – 57 cases (23.7%). Bone marrow infiltration was the most frequent reason for Stage IV disease (53 patients, 22% of the total cases) [Table 5]. Other disease sites leading to Stage IV disease were: liver – 9 cases, malignant ascites – 4, malignant pleural effusion – 3, multiple extranodal sites – 6, multifocal bone involvement – 1, brain – 4, and spine – 4 cases. Fluid cytology was positive in 41 cases (ascites 22, pleural fluid 19).
Table 4: Ann Arbor stage distribution of 241 cases

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Table 5: Distribution of Ann arbor Stage IV patients based on site of involvement, 84 cases

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  Discussion Top

NHL, despite being the most common lympho-hemopoietic malignancy in India, has lower ASR (0.8–5.1 males, 0.6–3.1 females) than that seen in the USA (16.1 males, 10.8 females).[7] Epidemiological features, clinical presentation, and histological subtypes of various types of NHL analyzed in this study revealed many differences from the Western data. These include younger median age, higher male-female ratio, head and neck as the most common extranodal site of disease, diffuse large cell as the most common histology, and higher frequency of Stage IV disease.

The median age of 47 years in the study is a decade earlier than reported in the Western literature.[7],[8],[9] Two earlier studies from AIIMS had reported the median age of 45 and 50 years, respectively.[1],[10] The reason for this earlier occurrence of NHL in India remains unexplained. However, many reasons have been suggested for this.[11] It is speculated that increased frequency of infectious diseases and chronic antigenic stimulation may be responsible. Indians are more exposed to infectious diseases at an early age, and this has been proposed as a reason for early peak (1st and 2nd decade) of Hodgkin's disease in India;[12] whether this applies to NHL also, remains unanswered. Different age structure in India (40% population <15 years compared to 21% in the west) may also be responsible for early median age.[11] Other possible reasons could be as follows: Different genetic makeup of Indians and socioeconomic factors with older people not reporting for treatment.[11]

Although males seem to be affected more than females throughout the world, the ratio of 2.2:1 in this study is higher compared to 1.5:1 reported in this west.[13],[14] Garg et al. had also reported higher male – female ratio (4.5:1) at our center.[10] Social structure-favoring males might be a factor for more male prevalence of NHL in males in India, though the exact reasons are not clear.

Extranodal non-Hodgkin's lymphoma

Extranodal NHL accounts for 44.20% of NHL cases in our series, which is comparable to the reported literature (24%–48%). However, the frequency of head and neck region NHL is higher in our study (50% of extra nodal NHL, 22% of all NHL). In the west, GIT is the most common site of extra nodal disease.[15] Our results are similar to Japanese and Chinese series; in these countries also, head and neck region is the most common extranodal site.[12] However in Singapore, GIT is the most common site as is the case in the West. The reasons for these variations need to be discovered.


There is a lower frequency of follicular small cleaved cell NHL (6.2%) in the present study compared to the west (22.5%) and higher frequency (60.58%) of diffuse large cell NHL than reported in the west (19.7%).[15] This is consistent with other studies from India and Asia, which also report lower frequency (3.4%–13.2%) of follicular NHL.[12] At our center Garg et al. had earlier reported 13.4% frequency of follicular NHL.[10] At TMH Bombay, the almost similar figure of 11.4% has been reported.[16] Follicular NHL formed only 6.3% of all NHL at Chang Gung Memorial Hospital, Taiwan,[12] 2.8% in Thailand,[17] 1.1% in Egypt [18] and 2.1% in Lebanon.[19] The incidence of follicular lymphomas continues to be lower in Asians even after they immigrate to the USA, subsequent generations, however, record higher incidence suggesting an environmental influence.[20] Histological progression from follicular to the diffuse pattern has been reported;[21] thus, patients presenting late after the onset of symptoms may have an advanced disease and diffuse histological pattern. Although these factors may explain, to a limited extent, the high diffuse to the follicular ratio in India, there are other, yet unrecognized, factors responsible for this geographic variation in the histological pattern of NHL. Studies of Hodgkin's disease in India also reveal a high frequency of mixed cellularity and lymphocytic depletion types of lymphoma, known to be associated with poor prognosis, as compared with Western series that report a high incidence of nodular sclerosis type of Hodgkin's disease.[22] Whether genetic factors make our population more susceptible to diffuse lymphomas, which are associated with poor prognosis or whether viruses, carcinogens, nutritional, or socioeconomic factors are responsible, requires further study.

Stage distribution

Advanced stage (III/IV) is more frequent in our population than in the west (46). It may be either be due to late diagnosis due to poor socioeconomic status denying access to tertiary care or biological differences.

  Conclusion Top

There are differences in the epidemiology, clinical presentation, and histological subtypes of NHL in our population as compared to the Western countries, including young median age, more male to female ratio, more of head and neck NHL, more diffuse large cell histology and more of advanced stage.


It has a limitation in the form of being a retrospective study. Moreover, “Working Formulation” classification used in this study has now been replaced by the REAL and WHO classifications. In addition, there is a time delay in publication of this manuscript.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

Prakash G, Sharma A, Raina V, Kumar L, Sharma MC, Mohanti BK, et al. B cell non-Hodgkin's lymphoma: Experience from a tertiary care cancer center. Ann Hematol 2012;91:1603-11.  Back to cited text no. 1
Burkitt D, O'conor GT. Malignant lymphoma in African children. I. A clinical syndrome. Cancer 1961;14:258-69.  Back to cited text no. 2
Rambaud JC. Small intestinal lymphomas and alpha-chain disease. Clin Gastroenterol 1983;12:743-66.  Back to cited text no. 3
Catovsky D, Foa R. Adult T – Cell leukemia/lymphoma. In: Catovsky D, Foa R, editors. The Lymphoid Leukemias. London: Butterworths; 1990. p. 218.  Back to cited text no. 4
Lister TA, Crowther D, Sutcliffe SB, Glatstein E, Canellos GP, Young RC, et al. Report of a committee convened to discuss the evaluation and staging of patients with Hodgkin's disease: Cotswolds meeting. J Clin Oncol 1989;7:1630-6.  Back to cited text no. 5
Carbone PP, Kaplan HS, Musshoff K, Smithers DW, Tubiana M. Report of the committee on Hodgkin's disease staging classification. Cancer Res 1971;31:1860-1.  Back to cited text no. 6
Straus DJ, Filippa DA, Lieberman PH, Koziner B, Thaler HT, Clarkson BD, et al. The non-Hodgkin's lymphomas. I. A retrospective clinical and pathologic analysis of 499 cases diagnosed between 1958 and 1969. Cancer 1983;51:101-9.  Back to cited text no. 7
Anderson T, Chabner BA, Young RC, Berard CW, Garvin AJ, Simon RM, et al. Malignant lymphoma 1. The histology and staging of 473 patients at the national cancer institute. Cancer 1982;50:2699-707.  Back to cited text no. 8
Elias L. Differences in age and sex distributions among patients with non-Hodgkin's lymphoma. Cancer 1979;43:2540-6.  Back to cited text no. 9
Garg A, Dawar R, Agarwal V, Rustagi RK, Kochupillai V. Non-Hodgkin's lymphoma in Northern India. A retrospective analysis of 238 cases. Cancer 1985;56:972-7.  Back to cited text no. 10
Bhutani M, Vora A, Kumar L, Kochupillai V. Lympho-hemopoietic malignancies in India. Med Oncol 2002;19:141-50.  Back to cited text no. 11
Shih LY, Liang DC. Non-Hodgkin's lymphomas in Asia. Hematol Oncol Clin North Am 1991;5:983-1001.  Back to cited text no. 12
Boring CC, Squires TS, Tong T, Montgomery S. Cancer statistics, 1994. CA Cancer J Clin 1994;44:7-26.  Back to cited text no. 13
Glass AG, Karnell LH, Menck HR. The national cancer data base report on non-Hodgkin's lymphoma. Cancer 1997;80:2311-20.  Back to cited text no. 14
Yuen A, Jacobs C. Lymphomas of the head and neck. Semin Oncol 1999;26:338-45.  Back to cited text no. 15
Naresh KN, Srinivas V, Soman CS. Distribution of various subtypes of non-Hodgkin's lymphoma in India: A study of 2773 lymphomas using R.E.A.L. And WHO classifications. Ann Oncol 2000;11 Suppl 1:63-7.  Back to cited text no. 16
Piankijagum A, Pacharee P, Wasi P. Malignant lymphomas in Thailand: An analysis of 1095 cases. J Med Assoc Thai 1980;63:181-91.  Back to cited text no. 17
Nasr AL, Tawfik HN, el-Einen MA. Lymphoreticular tumors and leukemias in Egypt. J Natl Cancer Inst 1973;50:1619-21.  Back to cited text no. 18
Gédéon EM. Malignant lymphomas in Lebanon. J Med Liban 1973;26:501-12.  Back to cited text no. 19
Herrinton LJ, Goldoft M, Schwartz SM, Weiss NS. The incidence of non-Hodgkin's lymphoma and its histologic subtypes in Asian migrants to the United States and their descendants. Cancer Causes Control 1996;7:224-30.  Back to cited text no. 20
Garvin AJ, Simon RM, Osborne CK, Merrill J, Young RC, Berard CW, et al. An autopsy study of histologic progression in non-Hodgkin's lymphomas 192 cases from the national cancer institute. Cancer 1983;52:393-8.  Back to cited text no. 21
Dawar R, Mangalik A. Hodgkin disease: An analysis of 128 cases. Am J Hematol 1978;4:209-15.  Back to cited text no. 22


  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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