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Cancer Research and Treatment : Official Journal of Korean Cancer Association logoLink to Cancer Research and Treatment : Official Journal of Korean Cancer Association
. 2017 Mar 30;50(1):222–238. doi: 10.4143/crt.2017.093

Nationwide Statistical Analysis of Lymphoid Malignancies in Korea

Hyewon Lee 1, Hyeon Jin Park 2, Eun-Hye Park 3, Hee Young Ju 2, Chang-Mo Oh 3, Hyun-Joo Kong 3, Kyu-Won Jung 3, Byung-Kiu Park 2, Eunyoung Lee 1, Hyeon-Seok Eom 1,4,✉, Young-Joo Won 3,5,✉
PMCID: PMC5784621  PMID: 28361523

Abstract

Purpose

Regional differences in the incidence of lymphoid malignancies have been reported worldwide, but there has been no large-scale epidemiologic analysis in Korea. The aim of this study was to provide a nationwide population-based statistical analysis of Korean patients with lymphoid malignancies.

Materials and Methods

The Korea Central Cancer Registry analyzed the incidence and survival of patients with lymphoid malignancies from the Korean National Cancer Incidence Database. Diseases were grouped by clinically relevant categories based on the 2008 World Health Organization classification.

Results

Overall 65,948 lymphoid diseases were identified between 1999 and 2012. The incidence of most subtypes increased with age, except for precursor cell neoplasms. Male predominance (male:female ratio=1.28:1) was observed. In 2012, annual age-standardized incidence rates per 100,000 persons of Hodgkin’s lymphoma, mature B-cell neoplasm, mature T/natural killer (NK)–cell neoplasm, and precursor cell neoplasm were 0.46, 6.60, 0.95, and 1.50, respectively, and they increased yearly from 1999. Composite Hodgkin’s and non-Hodgkin’s lymphomas were extremely rare. Survival improvement estimated using 5-year relative survival rate was observed in patients with Hodgkin’s lymphoma (71.1%-83.0%), diffuse large B-cell lymphoma (49.5%-61.5%), plasma cell neoplasms (20.2%-36.9%), and lymphoblastic lymphoma/leukemia (41.5%-56.3%) between 1993 and 2012. However, survival rates of T/NK-cell lymphoma (excluding cutaneous T-cell lymphoma) ranged from 40.5%-43.5% during the study period. Survival rates decreased with age in most subtypes.

Conclusion

This report presented the subtype-specific statistical analysis of lymphoid malignancies in the Korean population, showing increasing incidences and survival rates in most subtypes.

Keywords: Epidemiology, Incidence, Survival, Hematologic neoplasms, Republic of Korea

Introduction

Lymphoid malignancies are a diverse group of neoplasms with different clinical presentations, histology, and biology. They are classified by the morphology, immunophenotype, cytogenetics, and clinical characteristics. The etiology of lymphoid neoplasms is not fully understood. Thus, combining an epidemiologic study with a biological study is helpful for understanding the pathogenesis of each disease.

Different incidences of lymphoid malignancies between regions have been reported [1]. Asian countries have been known to show a relatively lower incidence than the other countries in North America and Europe. In terms of the subtypes of lymphoid malignancies, it also varies in each region. For example, Asian populations show a higher incidence of mature T/natural killer (NK)–cell lymphoma and extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue type (mucosa-associated lymphoid tissue lymphoma), in contrast, Western population show higher incidence of follicular lymphoma and chronic lymphocytic leukemia (CLL) [2,3]. The distribution of lymphoma-associated viruses such as Epstein-Barr virus and human T-lymphoblastic virus-1 has been proposed as a risk factor for the high incidence of specific subtypes of mature T/NK-cell lymphoma in Asian people, but genetic factors may also affect the incidence [4,5].

The classification of hematologic malignancies mainly focused on morphologic and immunophenotypic characteristics before 1990s [6-8], but it has been modified to include cytogenetic characteristics which provide an improved understanding of tumor pathogenesis. The most recent classification of diseases for oncology, International Classification of Diseases for Oncology, third edition (ICD-O-3) was published in 2000 [9] and updated in 2013 to include the changes from the World Health Organization (WHO) classification published in 2008 [2]. Recent cancer registry studies have adopted this ICD-O-3, because it more accurately reflects our recent understanding of these diseases [10,11].

We have published nationwide statistical analyses of hematologic malignancies based on the Korea Central Cancer Registry (KCCR) in 2012 [12]. However, the data was not based on the ICD-O-3 classification. Therefore, to understand the comprehensive incidence and survival of lymphoid malignancies in Korea, we conducted present study with available ICD-O-3 data from the KCCR.

Materials and Methods

The Korean Ministry of Health and Welfare started the KCCR, a nationwide hospital-based cancer registry in 1980. In 1999, the KCCR expanded to include the entire population in the population-based cancer registry program. Incidence data on lymphoid malignancies between 1999 and 2012 was obtained from the Korean National Cancer Incidence Database (KNCIDB).

The classification of lymphoid malignancies was categorized to account for incidence and clinical characteristics based on the ICD-O-3 [9]. The codes for lymphoid malignancies were grouped into five clinically relevant categories based on the 2008 WHO classification [2]: Hodgkin’s lymphoma (HL), mature B-cell neoplasms, mature T-cell and NK-cell neoplasm, precursor cell neoplasm, and unknown type of lymphoid neoplasm (S1 Table).

The crude incidence rates (CR) and age-specific incidence rates of each subtype of lymphoid malignancy were calculated. The CR per 100,000 persons was calculated as an incidence rate based on the frequency of the disease in the entire population by dividing the total number of events (N) by the total number of person-year of observation (P) and multiplying the result by 100,000. The age-specific incidence rates per 100,000 within an age group (i) were calculated by dividing the number of incident cases observed in the age group (Ni) by the number of corresponding person-year of observation (Pi) and multiplying the result by 100,000. Age-standardized incidence rates (ASRs), a weighted average of crude age-specific rates, were calculated using the Segi’s world standard population [13]. Changes in the annual ASRs were examined by calculating the annual percentage change (APC) over a time period as (exp(b)–1)×100, where b is the slope of the regression of log(ASR) on a calendar year using the following linear regression equation: E(log(ASR)|year)=a+b year [14].

For the survival analyses, cases that were diagnosed as lymphoid malignancies and have available data in the KNCIDB between 1993 and 2012 were included. The patient status was followed until December 31, 2013. The relative survival rate (RSR) was estimated by comparing the observed survival of cancer patients with the expected survival of the general population [15]. Five-year RSR was calculated based on the Ederer II method using the algorithm created by Paul Dickman in SAS [16,17]. All analyses were performed using SAS ver. 9.2 (SAS Institute Inc., Cary, NC).

Results

1. Incidences of lymphoid malignancies in 2012

A total of 10,409 cases of hematologic malignancies occurred in 2012, including 6,638 lymphoid malignancies (63.8%) (3,732 men and 2,906 women, male:female ratio=1.28:1) (Fig. 1). This means that the proportions of lymphoid malignancy were 3.3% and 2.6% of all cancers in men and women, respectively. Among all lymphoid malignancies in men, mature B-cell neoplasms (71.8%) were the most frequent, followed by mature T-cell and NK-cell neoplasms (10.5%), and precursor cell neoplasms (8.7%). In women, mature B-cell neoplasms (74.5%) were the most frequent, followed by precursor cell neoplasms (8.8%), and mature T-cell and NK-cell neoplasms (8.4%).

Fig. 1.

Fig. 1.

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Incident cases of lymphoid malignancies in Korea, 2012. NK, natural killer; MDS, myelodysplastic syndrome; AML, acute myeloid leukemia; MPN, myeloproliferative neoplasm. a)Include one case of composite Hodgkin’s and non-Hodgkin’s lymphoma.

Patients with aged between 70 and 79 years the highest incidence of lymphoid malignancies in 2012, followed by those aged 50 to 59 years, and then 60 to 69 years (Fig. 2). The precursor cell neoplasms were the most prevalent disease type in patients aged group 0-19 years, whereas mature B-cell neoplasms were the most prevalent in those aged more than 20 years.

Fig. 2.

Fig. 2.

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Incident cases of lymphoid malignancies by age group in Korea, 2012. NK, natural killer. a)All lymphoid malignancies include one case of composite Hodgkin’s and non-Hodgkin’s lymphoma.

2. Changes in incidences of lymphoid malignancies between 1999 and 2012

The incident cases of each subtype of lymphoid malignancies and trends in CR and ASR between 1999 and 2012 are shown in Table 1. During the study period, 65,948 lymphoid malignancies were registered. The overall ASR of all lymphoid malignancies increased from 6.9 to 9.9 during the study period. The APC was 3.2% between 1999 and 2012, and it was statistically significant. The ASRs increased from 0.24 to 0.46 in HL (APC, 5.0%; p < 0.05), from 3.41 to 6.60 in mature B-cell neoplasm (APC, 5.6%; p < 0.05), from 0.47 to 0.95 in mature T-cell and NK-cell neoplasm (APC, 6.6%; p < 0.05), and from 1.33 to 1.50 in precursor cell neoplasm (APC, 1.4%; p < 0.05). The ASR of cases categorized as “unknown type lymphoid neoplasm” decreased from 1.44 to 0.41 (APC, –9.3%; p < 0.05).

Table 1.

Number of lymphoid malignancies and trend in crude incidence rates and age-standardized incidence rates

Site Total Year
 APC
1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
Hodgkin’s lymphoma Cases 2,651 119 133 147 143 158 204 157 176 204 217 220 247 262 264
CR 0.39 0.25 0.28 0.31 0.30 0.33 0.42 0.32 0.36 0.42 0.44 0.44 0.50 0.52 0.52
ASR 0.35 0.24 0.26 0.29 0.28 0.30 0.39 0.29 0.34 0.37 0.40 0.39 0.43 0.48 0.46 5.0a)
 Hodgkin’s lymphoma, nodular lymphocyte predominant Cases 62 < 5 < 5 < 5 < 5 5 < 5 < 5 < 5 < 5 < 5 8 9 6 5
CR 0.01 0.01 0.01 0.01 0.01 0.01 0.00 0.01 0.01 0.01 0.00 0.02 0.02 0.01 0.01
ASR 0.01 0.01 0.01 0.01 0.01 0.01 0.00 0.01 0.01 0.01 0.00 0.01 0.02 0.01 0.01 4.1
 Classical Hodgkin’s lymphoma Cases 2,589 115 130 143 140 153 202 154 172 200 215 212 238 256 259
CR 0.38 0.24 0.27 0.30 0.29 0.32 0.42 0.32 0.35 0.41 0.44 0.43 0.48 0.51 0.51
ASR 0.34 0.23 0.26 0.28 0.28 0.29 0.39 0.29 0.33 0.37 0.40 0.38 0.41 0.47 0.45 5.0a)
Mature B-cell neoplasms Cases 42,647 1,650 1,613 1,895 2,044 2,425 2,663 2,877 3,088 3,323 3,575 4,024 4,154 4,472 4,844
CR 6.24 3.50 3.39 3.96 4.25 5.02 5.49 5.91 6.32 6.76 7.24 8.10 8.33 8.92 9.62
ASR 5.09 3.41 3.26 3.71 3.89 4.46 4.76 4.95 5.16 5.34 5.55 6.01 6.05 6.30 6.60 5.6a)
 Chronic lymphocytic leukemia/Small lymphocytic lymphoma Cases 1,495 90 65 87 103 81 102 89 126 102 104 126 116 147 157
CR 0.22 0.19 0.14 0.18 0.21 0.17 0.21 0.18 0.26 0.21 0.21 0.25 0.23 0.29 0.31
ASR 0.18 0.19 0.13 0.17 0.20 0.15 0.18 0.15 0.20 0.16 0.16 0.18 0.16 0.20 0.20 1.0
 Immunoproliferative diseases Cases 310 7 8 20 16 14 15 20 20 27 30 32 27 36 38
CR 0.05 0.01 0.02 0.04 0.03 0.03 0.03 0.04 0.04 0.05 0.06 0.06 0.05 0.07 0.08
ASR 0.04 0.01 0.02 0.04 0.03 0.03 0.03 0.03 0.03 0.04 0.05 0.05 0.04 0.05 0.05 8.0a)
 Mantle cell lymphoma Cases 734 27 22 32 22 36 50 48 67 50 68 58 80 70 104
CR 0.11 0.06 0.05 0.07 0.05 0.07 0.10 0.10 0.14 0.10 0.14 0.12 0.16 0.14 0.21
ASR 0.09 0.06 0.04 0.06 0.04 0.07 0.09 0.08 0.11 0.08 0.10 0.08 0.11 0.09 0.13 7.1a)
 Follicular lymphoma Cases 1,498 76 57 74 89 92 77 69 102 107 124 128 132 175 196
CR 0.22 0.16 0.12 0.15 0.18 0.19 0.16 0.14 0.21 0.22 0.25 0.26 0.26 0.35 0.39
ASR 0.18 0.16 0.11 0.14 0.16 0.17 0.13 0.12 0.17 0.18 0.20 0.19 0.19 0.25 0.28 5.1a)
 Diffuse large B-cell lymphoma Cases 19,659 856 872 988 997 1,154 1,287 1,320 1,395 1,545 1,613 1,758 1,821 2,003 2,050
CR 2.88 1.81 1.83 2.06 2.07 2.39 2.65 2.71 2.85 3.14 3.26 3.54 3.65 4.00 4.07
ASR 2.34 1.75 1.74 1.92 1.88 2.10 2.29 2.27 2.32 2.47 2.50 2.63 2.65 2.82 2.77 4.0a)
 Burkitt’s lymphoma/Leukemia Cases 976 25 32 30 63 58 75 61 85 92 82 83 92 92 106
CR 0.14 0.05 0.07 0.06 0.13 0.12 0.15 0.13 0.17 0.19 0.17 0.17 0.18 0.18 0.21
ASR 0.16 0.06 0.09 0.08 0.16 0.14 0.18 0.14 0.19 0.20 0.18 0.20 0.23 0.21 0.25 9.6a)
 Marginal zone lymphoma Cases 6,716 100 73 96 193 370 379 476 519 507 632 790 790 876 915
CR 0.98 0.21 0.15 0.20 0.40 0.77 0.78 0.98 1.06 1.03 1.28 1.59 1.58 1.75 1.82
ASR 0.79 0.20 0.14 0.18 0.35 0.66 0.66 0.81 0.86 0.82 0.99 1.19 1.17 1.25 1.28 18.4a)
 B-Cell prolymphocytic leukemia Cases 32 0 0 0 0 0 < 5 0 < 5 < 5 < 5 7 8 5 < 5
CR 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.01 0.00 0.01 0.01 0.02 0.01 0.01
ASR 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.01 0.01 0.01 0.00 6.6
 Hairy cell leukemia Cases 58 < 5 < 5 6 < 5 < 5 < 5 < 5 < 5 < 5 6 8 6 6 < 5
CR 0.01 0.01 0.00 0.01 0.00 0.01 0.01 0.01 0.01 0.01 0.01 0.02 0.01 0.01 0.01
ASR 0.01 0.01 0.00 0.01 0.00 0.01 0.01 0.01 0.01 0.00 0.01 0.01 0.01 0.01 0.00 3.4
 Plasma cell neoplasms Cases 11,169 466 482 562 560 616 673 791 767 889 913 1,034 1,082 1,062 1,272
CR 1.63 0.99 1.01 1.17 1.16 1.28 1.39 1.62 1.57 1.81 1.85 2.08 2.17 2.12 2.53
ASR 1.30 0.98 0.99 1.12 1.07 1.14 1.19 1.34 1.26 1.39 1.37 1.48 1.48 1.40 1.63 3.7a)
Mature T-cell and NK-cell neoplams Cases 6,612 232 233 265 300 414 441 515 531 503 591 649 654 650 634
CR 0.97 0.49 0.49 0.55 0.62 0.86 0.91 1.06 1.09 1.02 1.20 1.31 1.31 1.30 1.26
ASR 0.82 0.47 0.46 0.51 0.58 0.77 0.82 0.91 0.92 0.86 0.97 1.05 0.98 0.99 0.95 6.6a)
 T lymphoma cutaneous Cases 744 21 22 18 28 34 36 49 57 49 83 89 87 91 80
CR 0.11 0.04 0.05 0.04 0.06 0.07 0.07 0.10 0.12 0.10 0.17 0.18 0.17 0.18 0.16
ASR 0.09 0.04 0.04 0.04 0.05 0.06 0.07 0.09 0.11 0.08 0.15 0.15 0.14 0.15 0.13 12.5a)
 Other T and NK- cell lymphomas Cases 5,868 211 211 247 272 380 405 466 474 454 508 560 567 559 554
CR 0.86 0.45 0.44 0.52 0.57 0.79 0.84 0.96 0.97 0.92 1.03 1.13 1.14 1.12 1.10
ASR 0.72 0.42 0.41 0.47 0.53 0.71 0.75 0.81 0.82 0.77 0.83 0.89 0.84 0.84 0.81 5.9a)
Precursor cell neoplams Cases 7,409 533 479 521 518 520 480 501 526 536 524 569 581 541 580
CR 1.08 1.13 1.01 1.09 1.08 1.08 0.99 1.03 1.08 1.09 1.06 1.15 1.16 1.08 1.15
ASR 1.35 1.33 1.19 1.31 1.30 1.31 1.22 1.26 1.35 1.37 1.35 1.46 1.50 1.44 1.50 1.4a)
 Lymphoblastic lymphoma Cases 749 46 37 52 52 53 58 38 63 45 47 54 66 60 78
CR 0.11 0.10 0.08 0.11 0.11 0.11 0.12 0.08 0.13 0.09 0.10 0.11 0.13 0.12 0.15
ASR 0.13 0.10 0.09 0.12 0.13 0.12 0.14 0.09 0.15 0.11 0.11 0.14 0.16 0.13 0.18 3.3a)
 Lymphoblastic leukemia Cases 6,660 487 442 469 466 467 422 463 463 491 477 515 515 481 502
CR 0.97 1.03 0.93 0.98 0.97 0.97 0.87 0.95 0.95 1.00 0.97 1.04 1.03 0.96 1.00
ASR 1.22 1.23 1.10 1.19 1.17 1.19 1.09 1.17 1.21 1.25 1.23 1.33 1.34 1.31 1.32 1.2a)
Composite Hodgkin’s and non-Hodgkin’s lymphoma Cases 11 0 < 5 < 5 0 0 0 0 0 < 5 0 < 5 0 < 5 < 5
CR 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.01 0.00 0.01 0.00 0.00 0.00
ASR 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 3.5
Unknown type lymphoid neoplasm Cases 6,618 699 668 661 601 455 494 434 431 478 337 339 320 386 315
CR 0.97 1.48 1.41 1.38 1.25 0.94 1.02 0.89 0.88 0.97 0.68 0.68 0.64 0.77 0.63
ASR 0.80 1.44 1.34 1.29 1.16 0.84 0.90 0.76 0.73 0.77 0.52 0.50 0.46 0.53 0.41 –9.3a)
All lymphoid malignancies Cases 65,948 3,233 3,127 3,490 3,606 3,972 4,282 4,484 4,752 5,047 5,244 5,804 5,956 6,313 6,638
CR 9.65 6.85 6.58 7.29 7.49 8.22 8.83 9.21 9.72 10.27 10.61 11.69 11.94 12.60 13.18
ASR 8.41 6.89 6.51 7.11 7.21 7.68 8.09 8.17 8.50 8.71 8.80 9.42 9.42 9.74 9.93 3.2a)
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APC, annual percentage change; CR, crude incidence rate; ASR, age-standardized incidence rate; NK, natural killer.

a)

The annual percent change is statistically different from zero (p < 0.05).

3. Estimated RSRs of lymphoid malignancies

The 5-year RSRs of patients with lymphoid malignancies in 5-year intervals (1993-1997, 1998-2002, 2003-2007, and 2008-2012) are shown in Table 2. HL was associated with better survival than the other disease categories. Decreasing survival with age was observed in most disease types of lymphoid malignancies, with poor prognoses in elderly patients. Especially in patients with precursor cell neoplasms, abrupt decrease in survival rates were observed between pediatric patients (aged 0-14 years), adolescents and young adults (aged 15-34 years), and adults (aged 35 years or more).

Table 2.

Five-year relative survival rates of lymphoid malignancies by age group in Korea

Site Age (yr) Year
1993-1997
 1998-2002
 2003-2007
 2008-2012
Cases Relative survival Cases Relative survival Cases Relative survival Cases Relative survival
Hodgkin’s lymphoma Total 473 71.1 649 72.9 862 79.1 1,135 83.0
0-14 39 87.4 49 94.0 64 95.4 60 91.7
15-34 167 83.1 226 88.8 306 89.8 420 93.4
35-49 108 78.5 138 75.2 176 86.4 192 93.3
50-64 100 53.3 141 58.3 180 74.4 247 80.0
65-79 55 43.6 87 42.7 118 45.2 189 55.5
≥ 80 < 5 - 8 - 18 - 27 37.0
 Hodgkin’s lymphoma, nodular lymphocyte predominant Total < 5 - 17 - 17 - 30 92.5
 Classical Hodgkin’s lymphoma Total 469 71.0 632 72.8 845 79.0 1,105 82.7
0-14 39 87.4 49 94.0 64 95.4 59 91.6
15-34 167 83.1 223 88.7 299 89.6 409 93.2
35-49 106 78.1 131 73.8 175 86.3 184 93.8
50-64 98 53.3 136 58.9 173 74.4 239 80.2
65-79 55 43.6 85 42.4 116 44.8 187 54.5
≥ 80 < 5 - 8 - 18 - 27 37.0
Mature B-cell neoplasms Total 4,339 42.8 8,413 47.9 13,590 58.7 19,601 63.8
0-14 136 67.8 188 81.5 213 79.9 262 87.1
15-34 495 57.7 704 68.8 996 84.8 1,164 87.6
35-49 889 54.3 1,702 62.6 2,656 76.1 3,454 81.3
50-64 1,676 40.3 3,097 47.0 4,602 62.3 6,638 69.9
65-79 1,057 26.8 2,457 31.7 4,530 41.1 6,930 48.4
≥ 80 86 28.4 265 21.1 593 25.2 1,153 29.6
 Chronic lymphocytic leukemia/Small lymphocytic lymphoma Total 306 53.1 414 53.7 469 63.0 601 73.7
0-14 14 - < 5 - 0 - < 5 -
15-34 24 - 15 - < 5 - 9 -
35-49 58 70.4 67 70.0 49 82.7 67 89.2
50-64 111 57.0 156 58.5 163 67.3 199 88.0
65-79 89 30.4 146 45.9 225 58.0 277 63.3
≥ 80 10 - 26 6.6 28 41.4 47 45.3
 Immunoproliferative diseases Total 40 41.3 60 37.4 94 60.7 153 54.0
 Mantle cell lymphoma Total 40 60.8 118 53.0 237 41.4 355 52.4
0-14 < 5 - 0 - 0 - 0 -
15-34 5 - 8 - 5 - < 5 -
35-49 8 - 22 - 32 66.6 34 75.7
50-64 12 - 53 45.9 91 43.9 138 54.1
65-79 13 - 34 45.4 99 27.4 154 49.6
≥ 80 < 5 - < 5 - 10 - 27 0.0
 Follicular lymphoma Total 298 64.5 338 71.4 419 79.8 706 88.3
0-14 7 - 7 - < 5 - < 5 -
15-34 55 69.6 39 85.0 53 100.3 67 93.6
35-49 80 71.6 103 84.7 117 81.4 207 95.1
50-64 101 62.2 111 67.5 155 79.8 250 91.0
65-79 51 57.8 70 49.8 84 63.2 161 74.6
≥ 80 < 5 - 8 - 7 - 17 -
 Diffuse large B-cell lymphoma Total 2,213 49.5 4,413 52.9 6,377 59.1 8,574 61.5
0-14 60 68.5 82 81.8 69 79.8 88 84.9
15-34 347 55.4 499 65.6 538 80.6 611 81.5
35-49 519 57.6 980 63.7 1,303 72.6 1,456 77.6
50-64 783 49.0 1,532 53.7 2,058 64.2 2,701 70.2
65-79 461 34.5 1,165 37.1 2,089 43.7 3,116 47.2
≥ 80 43 36.5 155 28.8 320 23.0 602 27.1
 Burkitt’s lymphoma/Leukemia Total 81 52.6 168 66.4 364 57.8 439 62.8
0-14 47 70.3 90 83.4 126 79.4 155 87.0
15-34 15 - 24 - 72 55.7 73 80.9
35-49 5 - 15 - 49 59.8 81 47.8
50-64 10 - 24 - 77 44.5 66 38.0
65-79 < 5 - 13 - 36 12.6 58 24.3
≥ 80 < 5 - < 5 - < 5 - 6 -
 Marginal zone lymphoma Total 59 90.3 548 85.7 2,165 95.0 3,808 98.2
0-14 0 - < 5 - 10 - 10 -
15-34 16 - 79 92.8 279 97.8 364 99.2
35-49 15 - 174 90.2 687 97.9 1,095 99.1
50-64 21 - 188 88.2 747 96.6 1,513 97.9
65-79 7 - 96 68.9 415 85.0 754 97.7
≥ 80 0 - 7 - 27 86.5 72 89.3
 B-Cell prolymphocytic leukemia Total 0 - 0 - 6 - 25 57.0
 Hairy cell leukemia Total 11 - 13 - 16 - 26 69.8
 Plasma cell neoplasms Total 1,291 20.2 2,341 23.7 3,443 32.6 4,914 36.9
0-14 < 5 - < 5 - < 5 - < 5 -
15-34 30 57.1 37 62.5 40 85.3 35 82.1
35-49 194 29.5 326 37.1 401 50.6 498 52.0
50-64 621 20.2 1,009 25.2 1,275 38.4 1,714 44.2
65-79 417 12.2 904 16.1 1,538 23.1 2,301 29.5
≥ 80 27 22.8 64 6.0 186 11.9 365 18.8
Mature T-cell and NK-cell neoplasms Total 442 46.4 1,275 46.4 2,267 44.6 2,979 50.4
0-14 32 56.4 51 82.4 104 67.4 94 74.8
15-34 89 56.5 218 57.1 364 60.1 408 74.3
35-49 126 46.8 322 52.1 554 50.6 667 60.3
50-64 126 43.0 384 40.1 672 43.1 873 48.4
65-79 59 32.8 272 34.7 505 26.6 791 32.8
≥ 80 10 - 28 24.5 68 15.1 146 23.4
 T lymphoma cutaneous Total 63 59.8 128 72.6 217 82.5 419 87.7
0-14 < 5 - 7 - 13 - 21 -
15-34 11 - 31 77.7 58 88.2 107 95.6
35-49 21 - 32 72.7 66 82.8 115 92.7
50-64 15 - 30 69.7 49 84.6 95 91.6
65-79 10 - 27 64.2 26 61.6 67 69.6
≥ 80 < 5 - < 5 - 5 - 14 -
 Other T and NK-cell lymphomas Total 379 44.2 1,147 43.5 2,050 40.5 2,560 44.2
0-14 29 51.9 44 79.6 91 62.7 73 67.3
15-34 78 51.6 187 53.7 306 54.8 301 66.7
35-49 105 46.5 290 49.8 488 46.3 552 53.6
50-64 111 41.2 354 37.5 623 39.9 778 43.0
65-79 49 31.7 245 31.5 479 24.6 724 29.4
≥ 80 7 - 27 25.3 63 13.4 132 24.8
Precursor cell neoplasms Total 2,111 41.5 2,489 48.7 2,517 52.8 2,691 56.3
0-14 1,161 61.6 1,286 71.3 1,254 77.8 1,189 82.7
15-34 524 21.7 618 32.5 563 39.7 595 50.1
35-49 203 13.0 289 21.0 321 24.6 407 33.0
50-64 164 9.0 175 15.0 221 15.9 307 20.7
65-79 57 6.8 113 3.2 142 6.2 174 13.5
≥ 80 < 5 - 8 - 16 - 19 -
 Lymphoblastic lymphoma Total 101 43.0 222 45.8 249 51.8 294 54.4
0-14 44 59.2 88 66.0 92 75.1 86 75.2
15-34 35 31.6 91 36.4 93 47.5 113 54.4
35-49 11 - 23 - 24 - 48 43.2
50-64 8 - 11 - 28 29.9 23 -
65-79 < 5 - 9 - 9 - 21 -
≥ 80 0 - 0 - < 5 - < 5 -
 Lymphoblastic leukemia Total 2,010 41.4 2,267 49.0 2,268 52.9 2,397 56.5
0-14 1,117 61.7 1,198 71.6 1,162 78.1 1,103 83.3
15-34 489 21.0 527 31.8 470 38.2 482 49.2
35-49 192 12.2 266 19.8 297 25.2 359 31.6
50-64 156 7.4 164 15.3 193 13.9 284 20.9
65-79 54 7.2 104 2.4 133 6.6 153 11.0
≥ 80 < 5 - 8 - 13 - 16 -
Composite Hodgkin’s and non-Hodgkin’s lymphoma Total 0 - < 5 - < 5 - 6 -
Unknown type lymphoid neoplasm Total 3,227 47.1 2,957 52.7 1,935 52.1 1,435 50.2
0-14 168 60.3 124 72.7 69 75.5 27 84.2
15-34 522 52.8 369 65.6 194 76.5 98 81.4
35-49 698 58.9 649 67.2 357 70.3 202 78.0
50-64 1,064 45.6 897 54.5 507 60.7 329 66.2
65-79 713 31.2 784 32.8 619 33.2 551 35.8
≥ 80 62 21.3 134 23.0 189 16.8 228 13.5
All lymphoid malignancies Total 10,592 45.3 15,784 49.9 21,173 56.7 27,847 61.7
0-14 1,536 62.5 1,698 73.5 1,704 78.0 1,632 83.3
15-34 1,797 48.1 2,135 58.6 2,423 70.6 2,686 78.0
35-49 2,024 52.6 3,101 59.2 4,066 68.5 4,924 74.8
50-64 3,130 40.9 4,694 47.0 6,182 58.7 8,394 66.0
65-79 1,941 28.5 3,713 31.5 5,914 38.2 8,637 45.6
≥ 80 164 25.4 443 21.1 884 22.4 1,574 26.6
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-, statistic not displayed due to less than 25 cases; NK, natural killer.

4. Changes in the RSRs by major subtypes

The 5-year RSRs of patients with lymphoid malignancies continually increased from 1993 to 2012, from 45.3% to 61.7%, with an increment of 16.4% between these years. The 5-year RSR for most lymphoid malignancies was improved: from 71.1% to 83.0% in HL, from 42.8% to 63.8% in mature B-cell neoplasms, and from 41.5% to 56.3% in precursor cell neoplasms.

Trends in the RSRs of several major subtypes that are clinically important and accessible in our database are shown in Fig. 3. Yearly improvement of survival outcome was observed in HL, diffuse large B-cell lymphoma (DLBCL), multiple myeloma (MM), lymphoblastic lymphoma, and acute lymphoblastic leukemia. However, survival improvement was not evident in peripheral T-cell lymphomas or extranodal NK/T-cell lymphomas between 1993 and 2012.

Fig. 3.

Fig. 3.

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Trend in relative survival rate of lymphoid malignances between 1993 and 2012 in Korea. ICD-O-3 codes are as follows. (A) Hodgkin’s lymphoma 9659, 9650, 9661, 9662, 9651, 9663, 9664, 9665, 9667, 9652,9653, 9654, 9655. (B) Diffuse large B-cell lymphoma 9675, 9678, 9679, 9680, 96849684. (C) Multiple myeloma 9732. (D) Peripheral T-cell lymphoma, except NK/ T-cell lymphoma 9702, 9705, 9714, 9716, 9717. (E) Extranodal NK/T-cell lymphoma, nasal type 9719. (F) Lymphoblastic lymphoma 9728, 9729, 9727. (G) Acute lymphoblastic leukemia 9836, 9837, 9835. (H) All lymphoid malignancies. ICD-O-3, International Classification of Diseases for Oncology, third edition.

Discussion

Here, we presented the first comprehensive epidemiologic analysis for lymphoid malignancies in the Korean population. The incidence of lymphoid malignancies increased yearly between 1999 and 2012. In most subtypes except precursor cell neoplasms, the incidences in adults and elderly patients were higher than those in pediatric patients. Relative survival improved during the study period in lymphoid malignancies. However, poor survival outcomes in elderly patients were observed in most subtypes except in indolent diseases such as marginal zone lymphoma.

The incidence of most subtypes in Korea was low, with an ASR less than one per 100,000 except for DLBCL (2.34) and plasma cell neoplasms (1.30). This incidence is quite low compared to data from other countries as we expected based on previous reports of differences in incidences of lymphoid malignancies between countries or ethnic groups (Table 3) [11,14,18,19]. The incidence of several subtypes, including follicular lymphoma (ASR, 0.18) and CLL (ASR, 0.18), is lower in Korea than in Western countries. In contrast, the incidence of extranodal NK/T-cell lymphoma, nasal type was relatively high (ASR, 0.22). CLL/small lymphocytic lymphoma (SLL) is the second most common subtype of mature B-cell malignancies in Europe (26%); however, it is rare in Korea (3.4%). Follicular lymphoma was also rare in Korea compared to in European countries (3.4% vs. 11% of mature B-cell malignancies) [11]. The proportions of CLL/SLL and follicular lymphoma among B-cell non-Hodgkin’s lymphoma (NHL) in the United States were 19.6% and 12.3%, respectively [14]. Although we cannot directly compare the ASRs from our data with those of other registry-based incidences, there are subtype-specific differences in the Korean population compared to foreign data. An increasing trend in the incidence of HL and NHL was observed in Korea, which is similar to Japan [19], but not the United States.

Table 3.

International comparison of age-standardized incidence rates of lymphoid malignancies

Europe (HAEMACARE)a)
 The United States (SEER White)b)
 The United States (SEER Asian)b)
 Hong Kongb)
 Japanc)
 KCCRd)
2000-2002 2001-2010 2001-2010 2001-2010 2008 1999-2012
HL 2.41 2.91 1.28 0.75 0.5 0.35
CLL/SLL 3.79 4.75 1.06 0.52 0.1 0.18
DLBCL 3.13 5.59 4.37 3.26 2.5 2.34
FL 1.92 3.17 1.33 0.75 0.1 0.18
MCL NA 0.63 0.24 0.20 0.1 0.09
MZL NA 1.53 1.18 0.74 0.5 0.79
BL NA 0.42 0.28 0.27 0.12 0.16
PCN 4.62 4.03 2.54 1.99 1.5 1.30
Extranodal NK/T NA 0.06 0.12 0.25 0.08 0.22
ALCL NA 0.32 0.20 0.18 0.11 0.11
AITL NA 0.10 0.13 0.12 0.12 0.10
PTCL-NOS NA 0.30 0.28 0.27 0.25 0.26
ALL/LBL 1.42e) 1.7f) NA 1.1 1.22
All lymphoid 24.50 28.55 16.11 11.22 NA 8.41
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All rates expressed per 100,000 person-years. SEER, Surveillance, Epidemiology, and End Results; KCCR, Korea Central Cancer Registry; HL, Hodgkin’s lymphoma; CLL/SLL, chronic lymphocytic leukemia/small lymphocytic lymphoma; DLBCL, diffuse large B-cell lymphoma; FL, follicular lymphoma; MCL, mantle cell lymphoma; NA, not available; MZL, marginal zone lymphoma; BL, Burkitt’s lymphoma/leukemia; PCN, plasma cell neoplasm; NK, natural killer; ALCL, anaplastic large cell lymphoma; AITL, angioimmunoblastic T-cell lymphoma; PTCL-NOS, peripheral T-cell lymphoma, not otherwise specified; ALL, acute lymphoblastic leukemia; LBL, lymphoblastic lymphoma.

a)

Data from European HAEMACARE project [10],

b)

Ageadjusted to the World Health Organization’s World Standard Population (2000-2025) [21],

c)

Age-standardized to the world population. Estimated values from the published figures [22],

d)

Weighted averages of crude age-specific rates, calculated using Segi’s world standard population (presented data),

e)

This rate includes lymphoblastic lymphomas,

f)

From SEER data including all ethnic groups. Age-adjusted to the 2,000 U.S. standard population [23].

Comprehensive subtype-specific analysis in Asia is limited so far. A recent study performed in Hong Kong showed differences between Hong Kong and the United States [18]. The authors compared the incidences of lymphoid malignancies between the East Asian and white populations from Surveillance, Epidemiology, and End Results (SEER) data, and found that the age-adjusted incidence of most subtypes was < 1 per 100,000 in the Hong Kong population, except for DLBCL (3.26) and plasma cell neoplasms (1.99). The incidences of follicular lymphoma and CLL were 0.75 and 0.52, respectively, which was quite high compared to the incidences in our data (0.18 and 0.18). Rates in Asians from SEER data were generally intermediate compared to the rates in SEER Whites. Similar to our data, the incidence of extranodal T/NK-cell lymphoma, nasal type was much higher in Hong Kong (0.25) than in the United States (SEER White) (0.06). However, the number of Asian population in this analysis was relatively small compared to our data, with fewer than 10,000 cases in the Asian group, and survival data were lacking.

To our knowledge, this is the first population-based and subtype-specific survival analysis of hematologic malignancies in Asia. Comprehensive analysis based on subtypes defined by ICD-O-3 code is more useful than past population-based studies that divided lymphoid diseases in to broad categories such as ‘non-Hodgkin’s lymphoma’ or ‘leukemia’ [20].

The multicenter retrospective analysis in Korea by Won et al. [21] previously showed that the overall survival rate of classical HL with a median follow-up of 30 months was 80.2%. It did not include pediatric patients under the age of 16 years. In our KCCR data, the 5-year survival rate was 82.7% in 2008-2012. The overall survival outcome of HL was favorable. However, the survival rate of elderly patients over 65 years significantly decreased to 37%-54.4%. The poor outcome of elderly patients may be due to unfavorable tumor biology and underlying comorbidities as well as the toxicity of current standard chemotherapy such as anthracyclines and bleomycin [22,23]. The introduction of less toxic but effective treatment would likely improve survival outcomes, especially in elderly patients, and the results of such treatment regimens could be evaluated in a future update of KCCR analyses.

We also observed marked survival improvement in patients with DLBCL between the pre-rituximab and post-rituximab era: 5-year RSRs of 49.5% to 61.5% from 1993-1997 to 2008-2012, respectively. Rituximab, a monoclonal antibody that binds to CD20 on B cells and induces apoptosis of lymphoma cells, was approved in November 2003 by the Ministry of Food and Drug Safety (MFDS) in Korea. The influence of rituximab-containing chemoimmunotherapy on DLBCL survival has been reported [24]. In addition, rituximab has been approved for various indications in NHLs other than DLBCL in the United States [25]. In our data, survival rates of follicular lymphoma also increased during the study period. With the broadened indication of rituximab in Korea for other NHLs such as mantle cell lymphoma and marginal zone lymphoma, we can expect better outcomes in the future data, although there were no significant improvements of survival in the present data.

For other T- and NK-cell lymphomas, except cutaneous T-cell lymphoma, there were no evident changes in survival rates during the study period (5-year RSR, 44.2% to 44.2% between 1993-1997 and 2008-2012, respectively). This result is in line with the unsatisfactory results of clinical trials for the disease categories, except for the paradigm shift in the management of extranodal NK/T-cell lymphoma, nasal type. In localized diseases, concomitant/sequential chemo

therapy and radiotherapy became standard therapy because radiotherapy alone was not adequate due to systemic relapse [26]. For advanced cases, systemic chemotherapy containing L-asparaginase and drugs unaffected by P-glycoprotein was indicated [27]. In subtype-specific analyses, survival of extranodal NK/T-cell lymphoma, nasal type, improved, revealing a 5-year RSR of 49.9% for all age groups in 2008-2012 (n=869) compared to 45.8% in 2003-2007 (n=670) and 46.5% in 1998-2002 (n=314) (Fig. 3). The RSR in 1993-1997 seems to be superior, but this result might be due to a limitation of the registry; the registry did not cover the entire population at that time, so the number of cases was relatively insufficient (153 cases in 1993-1997). The survival benefits from the current therapy for extranodal NK/T-cell lymphoma, nasal type, needs to be confirmed in future analysis.

The standard treatment of MM also changed during the study period. Autologous stem cell transplantation was introduced in early 1990s. In addition, thalidomide, bortezomib, and lenalidomide were approved by MFDS in April 2006, March 2006, and December 2009, respectively. We found that the 5-year RSR of patients with plasma cell neoplasms changed from 20.2% to 36.9% from 1993 to 2012, respectively. This rate is still unsatisfactory, and it is lower than the RSR in the United States (48.5%) between 2006 and 2012 [14], but an increasing trend in survival rates in Korea is encouraging for such an ‘incurable disease.’

The survival rates of acute lymphoblastic leukemia/lymphoma showed improving trends based on the year of diagnosis, with 5-year RSR of all age groups reaching 56.3% in 2008-2012. Age at diagnosis significantly influenced the survival of this disease. The 5-year RSR in pediatric patients (aged 0-14 years) is 82.7%, but it falls dramatically in young adults (50.1%, aged 15-34 years) and adults (33%, aged 35-49 years). Poor prognosis of adult acute lymphoblastic leukemia /lymphoma is historically well known, and the factors associated with this difference in outcome include the poorer biology of the leukemia, the lower compliance of patients (physically and emotionally), differences in the therapeutic approaches, and the lower rates of enrollment in clinical trials [28-30]. Efforts to improve outcomes in adults include development of pediatric-inspired chemotherapy protocols for young adults and the combination of tyrosine kinase inhibitors, such as imatinib and dasatinib with conventional chemotherapy for Philadelphia-positive disease. Well-designed and clinical trial-based treatment protocols for adult patients should be established in Korea.

We reported the subtype-specific incidence and survival of lymphoid malignancies. Our research showed increasing incidence and survival rates based on the year of diagnosis in most subtypes. In addition, the survival rates of most subtypes (except for indolent disease) decreased dramatically with age. The strength of our study is that these data were analyzed in clinically meaningful disease categories. Additionally, this is a good example for refining and utilizing data from pre-existing cancer registry. If we can integrate more detailed information such as immunophenotypes, genetic abnormalities, and treatment information, to the registry, the quality of data on hematologic malignancies will improve. The qualified registry can provide practical evidence to determine whether advances in diagnosis and treatment can improve cancer survival.

Acknowledgments

This work was supported by a research grant from the National Cancer Center (1610200).

Footnotes

Conflict of interest relevant to this article was not reported.

Electronic Supplementary Material

Supplementary materials are available at Cancer Research and Treatment website (http://www.e-crt.org).

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