Global patterns and trends in the incidence of non-Hodgkin lymphoma

Abstract

Purpose
Despite an increasing understanding of the pathology and genetics of non-Hodgkin lymphoma (NHL), global reports on variations in the incidence of NHL remain limited in their number and scope.

Methods
To provide a situation analysis, national incidence estimates for NHL in 185 countries for the year 2018 were obtained from the GLOBOCAN database. We also used recorded incidence data from Cancer Incidence in Five Continents (CI5) plus for years of diagnosis 1980–2012 to examine temporal trends.

Results
NHL ranked as the 5th to 9th most common cancer in most countries worldwide, with almost 510,000 new cases estimated in 2018. Observed incidence rates of NHL 2008–2012 varied markedly by world region: among males, rates were highest among Israel Jews [age-standardized (world) rate of 17.6 per 100,000), Australia (15.3), US whites (14.5), Canada (13.7), and Portugal (13.3)]. Where data were available, most populations exhibited stable or slightly increasing incidence rates; in North America, parts of Europe, and Oceania the rising incidence rates were generally observed until the 1990s, with a stabilization seen thereafter.

Conclusion
Marked variations in NHL incidence rates remain in populations in each world region. Special attention should be given to further etiological research on the role of endemic infections and environmental exposures, particularly in Africa, Asia, and Latin America. To permit internationally comparable statistics, an equal focus on addressing the quality of hematological information in population-based registries is also warranted.

Full text

Vol.:(0123456789)
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Cancer Causes & Control
https://doi.org/10.1007/s10552-019-01155-5
ORIGINAL PAPER
Global patterns andtrends intheincidence ofnon-Hodgkin
lymphoma
AdalbertoMiranda‑Filho1 · MarionPiñeros1· ArianaZnaor1· RafaelMarcos‑Gragera2· EvaSteliarova‑Foucher1·
FreddieBray1
Received: 22 August 2018 / Accepted: 6 March 2019
© Springer Nature Switzerland AG 2019
Abstract
Purpose Despite an increasing understanding of the pathology and genetics of non-Hodgkin lymphoma (NHL), global
reports on variations in the incidence of NHL remain limited in their number and scope.
Methods To provide a situation analysis, national incidence estimates for NHL in 185 countries for the year 2018 were
obtained from the GLOBOCAN database. We also used recorded incidence data from Cancer Incidence in Five Continents
(CI5) plus for years of diagnosis 1980–2012 to examine temporal trends.
Results NHL ranked as the 5th to 9th most common cancer in most countries worldwide, with almost 510,000 new cases
estimated in 2018. Observed incidence rates of NHL 2008–2012 varied markedly by world region: among males, rates were
highest among Israel Jews [age-standardized (world) rate of 17.6 per 100,000), Australia (15.3), US whites (14.5), Canada
(13.7), and Portugal (13.3)]. Where data were available, most populations exhibited stable or slightly increasing incidence
rates; in North America, parts of Europe, and Oceania the rising incidence rates were generally observed until the 1990s,
with a stabilization seen thereafter.
Conclusion Marked variations in NHL incidence rates remain in populations in each world region. Special attention should
be given to further etiological research on the role of endemic infections and environmental exposures, particularly in Africa,
Asia, and Latin America. To permit internationally comparable statistics, an equal focus on addressing the quality of hema-
tological information in population-based registries is also warranted.
Keywords Lymphoid neoplasms· Non-Hodgkin lymphoma· Population-based cancer registries· Global epidemiology
Introduction
Non-Hodgkin lymphoma (NHL) ranks as the tenth and
twelfth most frequent cancer in males and females world-
wide, respectively, with an estimated 509,590 new cases and
248,724 deaths in 2018 [1]. These malignancies arise from
the malignant transformation of mature and immature cells
of immune system, affecting either B lymphocytes (B cells,
representing around 86% of all NHL), and a smaller propor-
tion of T- and natural killer (NK) cells (14% in developing
regions) [2]. The classification of NHL is complex; knowl-
edge of both clinical features and genetic abnormalities is
essential to distinguish entities and provide accurate diag-
noses [3]. A large proportion of NHL diagnoses (e.g., 35%
in the UK) occur at older ages, with a peak incidence rate
at ages at 75 or older [4]; the frequency of NHL subtypes
varies by country [5]. Five-year survival estimates of 80%
are observed in high-income settings but vary according to
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s1055 2-019-01155 -5) contains
supplementary material, which is available to authorized users.
* Adalberto Miranda-Filho
mirandaa@fellows.iarc.fr
1 Section ofCancer Surveillance, International Agency
forResearch onCancer, 150 Cours Albert Thomas,
69372LyonCEDEX08, France
2 Epidemiology Unit andGirona Cancer Registry (UERCG),
Oncology Coordination Plan, Department ofHealth,
Autonomous Government ofCatalonia, Catalan Institute
ofOncology (ICO), Girona Biomedical Research Institute
(IDIBGI), University ofGirona, Girona, Spain

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subtype and age; survival is markedly lower in low- and
middle-income countries (LMIC) [6].
The incidence of NHL is associated with considerable
geographic and temporal variability worldwide, although
this inherent aetiological heterogeneity has helped uncover
few risk factors. Genetic determinants, including a family
history of NHL, have been implicated as a cause of NHL, as
have certain lifestyle and environmental factors, including
obesity and certain occupational exposures [7]. It has been
established that infections, particularly those associated with
Hepatitis C virus (HCV), Epstein–Barr virus (EBV), and
Helicobacter pylori (H. pylori) can increase or modulate
the risk of NHL [8]. While the risk of NHL is higher among
HIV-infected persons as a result of immunosuppression
[9], declines in the elevated risk have been reported from
some high-income settings in the post-antiretroviral therapy
(ART) era [10].
Even with an increasing understanding of the pathol-
ogy and genetics of NHL, global reports on the patterns
and trends of NHL remain rather limited in number and
scope. In part, this may reflect the underlying complexity
of evolving classification and diagnostic criteria that cancer
registries are tasked to comply with. This global overview
seeks to identify distinct patterns of incidence that may serve
to generate hypotheses for further investigation, as well as
inform cancer control. We focus on geographical and tem-
poral variations in NHL according to country, sex, and age
using the recorded data from population-based cancer reg-
istries (PBCR), alongside national estimates compiled at the
International Agency for Research on Cancer (IARC).
Methods
Data sources andpopulation
Estimates of NHL incidence for 185 countries in the year
2018 were extracted from IARC’s GLOBOCAN database
[1]. The methods of estimation are based on the most reli-
able sources of cancer incidence and mortality data avail-
able at national or subnational level. A detailed account of
the methods is provided by Ferlay and colleagues elsewhere
[11]. We examined the age profile of NHL according to the
Human Development Index (HDI) based on the predefined
cut-points: low (HDI < 0.5), medium (0.5 ≤ HDI < 0.8), high
(0.8 ≤ HDI < 0.9), and very high (HDI ≥ 0.9) [12].
The prevalence of HIV among adults aged 15 to 49 in 128
countries for the year 2010 was extracted from the WHO
Global Health Observatory [13], representing the percent-
age of the national population aged 15–49years and living
with HIV. These are visually correlated with age-standard-
ized NHL incidence rates as estimated in GLOBOCAN for
the year 2018 [11].
New cases of NHL and population-at-risk data were
extracted from successive volumes of Cancer Incidence in
Five Continents (CI5), a compendium of high-quality data
from population-based cancer registries (PBCR) worldwide
[14]. We extracted recorded incidence and population data
as reported in the latest volume of CI5 (volume XI) for 343
cancer registries in 62 countries worldwide, predominantly
for the years of diagnosis 2008–2012. We examined tem-
poral patterns of NHL in selected countries using the long-
standing high-quality cancer registries that were included in
the last six volumes of CI5 covering the period from 1980 to
2012, based on the data provided by population-based cancer
registries (PBCR) worldwide [15]. In the absence of national
coverage, an existing subnational registry or a pool of such
registries represented the relevant country (http://ci5.iarc.fr/
CI5-XI/Pages /regis try_summa ry.aspx).
To ensure comparability in the incidence between regis-
try populations in CI5, morphological groups of the Inter-
national Classification of Diseases for Oncology (ICD-O,
2000) were converted to the 10th revision of the Interna-
tional Classification of Diseases (ICD-10) and coded to C82-
86, C96 [16] as shown in Appendix I in supplementary file.
In order to ensure consistency in the included tumor types
between the successive volumes of CI5 malignant lym-
phoma, small B lymphocytic, NOS (9,670) was included in
our grouping of NHL, whereas NHL B-cell chronic lympho-
cytic leukemia/small lymphocytic lymphoma (9,823) was
excluded.
Statistical analyses
Age-specific incidence rates per 100,000 person-years were
estimated by country and sex and presented according to
HDI levels. Age-standardized rates (ASR) were weighted
using the World Standard population [17] and presented in
tabular form with corresponding 95% confidence intervals
[18]. The ASR for 2018 and its ranking in relation to other
cancer types were depicted in global maps. Time trends in
the ASR are presented by calendar year and sex. Analyses
were undertaken using R software 3.3.3 [19].
Results
Estimated incidence 2018
Figure1a illustrates the global variation in NHL incidence
rates in 2018 for both sexes combined; the corresponding
ASR by world region and sex are shown in Table1. Overall,
rates were consistently higher among males compared with
females, with sex ratios varying from 1.1 to 1.8 by region.
Among men, the highest incidence rates were observed in
Australia and New Zealand (16.4 per 100,000), Northern

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America (14.8 per 100,000), and in Northern Europe (13.5
per 100,000), while the lowest rates were seen in Middle
Africa (3.2 per 100,000) and Central America (4.60 per
100,000). A similar geographical pattern was observed in
females, with the highest rates observed in Northern Amer-
ica (10.4 per 100,000) and the lowest in Middle Africa (2.8
per 100,000). Figure1b shows the ranking of NHL by fre-
quency of new cases relative to other major cancers. Marked
differences were seen between and within regions world-
wide, with NHL ranking as the 4th leading cause of cancer
occurrence in Oman, Egypt, Bahrain, Qatar, and Sudan. In
a further 87 countries, NHL was the fifth to ninth most com-
mon cancer.
Observed incidence circa2008–2012
Figure2 shows the recorded national or subnational NHL
incidence rates circa 2008–2012 by country according to
HDI level. The number of cases and corresponding popula-
tions covered by the registries are tabulated in Table2. Inci-
dence rates of NHL varied tenfold, with NHL rates among
males highest in Israel Jews (17.6 per 100,000), Australia
Data source: Globocan 2018
Map production: IARC
World Health Organization
© WHO 2016. All rights reserved
The boundaries and names shown and the designations used on this map do not imply the expression of any opinion whatsoever
on the part of the World Health Organization concerning the legal status of any country, territory, city or area or of its authorities,
or concerning the delimitation of its frontiers or boundaries. Dotted and dashed lines on maps represent approximate borderlines
for which there may not yet be full agreement.
<3.0
3.0 - 4.5
4.6 - 5.8
5.9 - 8.5
>8.5
<5th
10th or greather
5th - 9th
(A)
(B)
Fig. 1 a Age-standardized (world) incidence rates (quintiles) of non-Hodgkin lymphoma, both sexes; b ranking of non-Hodgkin lymphoma by
frequency of new cases relative to other common cancers, both sexes (Source: GLOBOCAN, 2018)

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(15.3 per 100,000), US whites (14.5 per 100,000), Canada
(13.7 per 100,000), and Portugal (13.3 per 100,000). Among
females, similar patterns were observed with elevated rates
in Israel Jews (13.0 per 100,000) and Australia (12.3 per
100,000), followed by US whites (10.3 per 100,000) and
Canada (10.0 per 100,000). In males, incidence rates were
lowest in South Africa (1.6 per 100,000), Vietnam, and India
(3.5 and 3.6 per 100,000, respectively), with an analogous
profile observed among females, but with the lowest rates
ranging between 1 and 2 per 100,000.
Temporal patterns 1980–2012
Time trends in the NHL incidence rates by sex in selected
countries circa 1980–2012 are shown in Fig.3. In the major-
ity of countries, trends in incidence rates were either stable
or decreases among both males and females. The United
States, Canada, Australia, and New Zealand all exhib-
ited a rising incidence trend until the 1990s, followed by
a stabilization thereafter. Similar temporal patterns were
observed in Europe (e.g., in Austria, Croatia, Germany, Italy,
France, Spain, and Switzerland) and Asia (e.g., in Japan,
Korea, India, Philippines, and Thailand).
HIV prevalence, Human Development Index,
andNHL incidence
Figure4a presents a graphic representation of HIV preva-
lence in 2010 and the estimated incidence of NHL in 2018,
both sexes combined. Figure4b shows the estimated inci-
dence of NHL in 2018, and the Human Development Index,
both sexes combined. Higher rates of NHL were common in
countries classified as very high HDI, while many countries
classified as low and medium HDI presented lower incidence
rates. The linear relation between the magnitude of the NHL
incidence rates and level of HDI appears confined to very
high HDI countries.
Discussion
In this population-based study, we provide a comprehen-
sive review of NHL incidence using national estimates in
185 countries for the year 2018, complemented by a more
detailed exposition of geographical and temporal variations
based on either national or subnational high-quality data
from population-based cancer registries included in the Can-
cer Incidence in Five Continents series. We report distinct
geographic patterns in NHL incidence by world region, HDI
level, sex, and age, with rates consistently higher among
males than females. As a disease entity, NHL ranks as the
fourth leading cause of cancer occurrence in Oman, Egypt,
Bahrain, Qatar, and Sudan, and as the fifth to ninth most
common cancer in a further 87 countries of the world. The
incidence trends were stable or increasing in most countries
where data were available; in the populations representing
North America, Europe, and Oceania, a pattern of rising
incidence until the 1990s, followed by a stabilization, was
commonly observed.
NHL comprises a wide range of cancers of the immune
system ranging from indolent to aggressive types [3] for
which the extent of clinical resources are a major factor in
assuring accurate diagnoses. The observed heterogeneity of
NHL incidence rates by human development level seen in
this study can thus be postulated to be driven by disparities
in health system infrastructure and the delivery of cancer
services, and consequently, the availability of diagnostic and
treatment facilities for cancer [20]. Diagnostic precision of
NHL requires excisional biopsy, followed by a pathologist
examination and the final classification, based on morphol-
ogy, immunophenotype, genetic, and clinical features [21,
22]. Such a process may be unattainable at present in some
Table 1 Estimated number of cases and age-standardized (world)
incidence rates of non-Hodgkin lymphoma by world region and sex.
Source: GLOBOCAN, 2018
asr age-standardized incidence rate (world)
a Male:female rate ratio
Males Females M:Fa
Cases ASR Cases ASR
World 284,713 6.7 224,877 4.7 1.4
Africa
Eastern Africa 8,489 5.7 6,758 4.1 1.4
Middle Africa 1,848 3.2 1,609 2.8 1.1
Northern Africa 9,136 8.9 7,297 6.8 1.3
Southern Africa 2,047 7.3 1,981 5.8 1.3
Western Africa 5,512 5.0 3,910 3.2 1.6
Americas
Northern America 44,838 14.8 36,523 10.4 1.4
Caribbean 1,417 5.7 1,265 4.6 1.2
Central America 3,908 4.6 3,147 3.4 1.4
South America 16,529 7.2 13,144 4.8 1.5
Asia
Eastern Asia 68,990 5.5 57,274 4.3 1.3
South-Eastern Asia 19,716 6.2 13,334 3.8 1.6
South Central Asia 27,052 3.0 16,572 1.8 1.7
Western Asia 8,462 7.1 6,295 5.1 1.4
Europe
Eastern Europe 11,628 5.9 12,179 4.4 1.3
Northern Europe 12,989 13.5 10,711 9.7 1.4
Southern Europe 14,143 10.0 12,187 7.4 1.4
Western Europe 23,627 12.5 17,654 7.9 1.6
Oceania
Australia/New Zealand 4,030 16.4 2,815 10.4 1.6

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LMIC, where advanced diagnostic techniques are not availa-
ble. The reported NHL incidence may thus also be subject to
some misclassification and under-reporting in these settings.
The heterogeneity of NHL incidence rates and trends is
also related to the prevalence and distribution of the under-
lying known and putative risk factors [20]. In Africa, parts
of South America, and Asia, the estimated incidence rates
could in part reflect the infectious origin of NHL. There is
accumulating evidence that EBV is linked to the etiology
of NHL [23]. EBV-positive diffuse large B-cell lymphoma
(DLBCL) is a category of NHL subtype included in the
WHO Blue Books since 2008 and represents between 5 and
15% of all DLBCLs worldwide [24]. These cases are more
common in the elderly, as they relate to the process of aging
that causes alterations in the immune system and the pro-
tracted latency of EBV infection [25]. Several other T-cell
and NK-cell NHL are classified as EBV-positive; these are
rarer types, that have been reported to occur more commonly
in less-resourced settings in Asia and among indigenous
populations in Latin America [26].
Males
Females
Low HDI Medium HDI
High HDI
Human Development Index
Very high HDI
1.61.0
3.52.3
3.62.1
4.33.1
4.53.2
4.52.9
4.83.4
5.03.8
5.13.6
5.34.0
5.45.1
5.54.2
5.53.9
5.75.0
5.84.1
6.05.9
6.46.1
6.44.6
6.54.1
6.63.2
6.64.8
6.75.1
6.95.4
7.05.2
7.25.1
7.25.2
7.45.6
7.55.4
7.67.2
7.65.9
7.76.0
7.76.5
7.75.1
7.96.1
8.05.2
8.76.5
8.76.1
9.05.8
9.14.9
9.26.6
9.47.3
9.
78
.6
10.26.8
10.36.9
10.
47
.4
10.47.0
10.
97
.3
14.5 10.0
11.3 10.6
11.
57
.9
11.
68
.8
12.
08
.6
12.
19
.1
12.
27
.9
12.
38
.2
12.
59
.0
12.
59
.0
12.
98
.9
12.
98
.6
13.
19
.2
13.
37
.7
13.
79
.8
11.3 7.5
15.3 11.1
15.3 10.3
17.6 13.0
16.7 12.3
20 18 16 14 12 10 8 6 4 2 0 2 4 6 8 10 12 14 16 18
South Africa
India
Viet Nam
Algeria
Philippines
Ukraine
China
Bulgaria
Russian Federation
Chile
Jordan
Kenya
Belarus
Jamaica
Poland
Saudi Arabia
Kuwait
Thailand
Republic of Korea
Iran (2008-2011)
Argentina
Malaysia
Latvia
Uganda
Turkey
Costa Rica
Croatia
Lithuania
Seychelles
Colombia
Slovakia
Ecuador
Bahrain
Slovenia
Brazil
Czech Republic
Japan
Estonia
Qatar
Austria
Puerto Rico
Cyprus
Uruguay
Brunei Darussalam
Spain
Germany
Iceland
USA: White
Malta
Switzerland
Peru
Belgium
Ireland
France
Netherlands
United Kingdom
Norway
Italy
Denmark
New Zealand
Portugal
Canada
USA: Black
Zimbabwe (2010-2012)
Australia
Israel: Jews
Israel
Age standardised incidence rates per 100000
20
Fig. 2 Age-standardized (world) incidence rates of non-Hodgkin lymphoma by world region and HDI in males and females circa 2008–2012
(Source: Cancer Incidence in Five Continents Volume XI)

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Table 2 Number of new cases of NHL, age-standardized (world) incidence rates (ASR), and 95% confidence intervals, based diagnoses circa
2008–2012. Source: Cancer Incidence in Five Continents, Volume XI
Number of
registries
Population
covered in
million
Population
covered (%)
Males Females M:F
Cases ASR 95% CI Cases ASR 95% CI
Africa
Zimbabwe (2010–2012) 1 4.4 30.9 202 15.3 12.8 17.8 181 11.0 9.2 12.9 1.4
Seychelles 1 0.1 80.3 13 7.5 3.3 11.8 14 7.2 3.2 11.2 1.1
Uganda 1 2.2 6.6 256 6.9 5.8 8.2 203 5.1 4.2 6.2 1.3
Kenya 1 3.1 7.6 214 5.4 4.5 6.5 154 4.1 3.3 5.1 1.3
Algeria 2 2.4 6.6 223 4.2 3.7 4.9 171 3.1 2.6 3.7 1.4
South Africa 1 1.0 2.1 24 1.5 0.9 2.2 27 1.0 0.6 1.4 1.5
America and Caribbean
US: white (NPCR)a1 232.5 95 132,200 14.4 14.4 14.6 109,428 10.0 7.4 7.6 1.4
Canada 12 26.1 76.8 14,051 13.71 13.5 14 11,591 9.8 9.7 10 1.4
Peru 1 5.6 19 1,480 11.6 11 12.2 1,327 8.7 8.3 9.2 1.3
US: black (NPCR)a1 21.5 51 12,007 11.1 11.1 11.4 10,240 7.4 10 10.1 1.5
Uruguaya1 3.4 100 1,103 10.2 9.6 10.9 949 6.8 6.3 7.3 1.5
Puerto Ricoa1 3.8 100 1,250 9.4 8.9 10 1,200 7.3 6.9 7.8 1.3
Brazil 6 3.8 1.9 738 7.9 7.4 8.6 635 5.2 4.8 5.7 1.5
Ecuador 5 6.0 40.2 1,181 7.6 7.2 8.2 1,095 6.5 6.1 7 1.2
Colombia 4 4.1 9.0 774 7.6 7.1 8.2 772 5.9 5.5 6.3 1.3
Costa Rica (2008–2011)a1 3.6 79.8 623 7.1 6.6 7.7 465 5.1 4.7 5.6 1.4
Argentina 5 5.2 12.5 902 6.6 6.2 7.1 785 4.8 4.5 5.2 1.4
Jamaica 1 0.5 18.8 72 5.6 4.3 7 73 5.0 3.8 6.2 1.1
Chile 4 1.7 10.1 263 5.3 4.7 6 227 3.9 3.4 4.5 1.3
Asia
Israela4 7.6 100 3,583 16.7 16.1 17.3 3,133 12.3 11.9 12.8 1.4
Israel: Jewsa4 5.7 75.4 3,155 17.5 16.9 18.2 2,773 12.9 12.5 13.5 1.4
Brunei Darussalam 1 0.2 47.4 36 10.2 6.8 13.8 30 6.9 4.4 9.5 1.5
Qatar 1 0.2 1.25 40 9.1 6.1 12.2 24 4.9 2.8 7.1 1.8
Japan 9 28.2 22.1 13,058 8.7 8.6 8.9 10,960 6.0 5.9 6.2 1.4
Bahrain 1 1.2 100 91 7.7 6.1 9.4 61 5.0 3.7 6.5 1.5
Turkey 8 12.1 16.8 2,321 7.1 6.9 7.5 1,826 5.0 4.8 5.3 1.4
Iran (2008–2011) 1 1.4 1.8 182 6.5 5.5 7.6 92 3.1 2.5 3.9 2.1
Malaysia 4 0.9 3.1 157 6.7 5.6 7.8 125 5.1 4.2 6.1 1.3
Thailand 7 11.6 17.3 2,045 6.4 6.1 6.7 1,692 4.5 4.3 4.8 1.4
Kuwait 3 3.6 100 416 6.3 5.5 7.2 251 6.1 5.2 7 1.0
Republic of Korea 8 49.6 100 14,203 6.4 6.4 6.6 10,437 4.1 4.1 4.2 1.6
Saudi Arabia 1 21.4 77.7 558 5.9 5.4 6.5 456 5.8 5.3 6.5 1.0
Jordan 1 6.1 3.2 590 5.3 4.9 5.9 517 5.1 4.6 5.6 1.1
China 36 63.0 4.7 11,291 4.8 4.7 4.9 8,534 3.4 3.4 3.5 1.4
Philippines 2 14.0 15.0 1,195 4.4 4.2 4.8 1,063 3.2 3 3.4 1.4
India 16 47.3 3.8 4,099 3.4 3.4 3.6 2,648 2.3 2.3 2.4 1.5
Vietnam 1 6.0 6.8 421 3.6 3.2 4 314 2.1 1.9 2.4 1.7
Eastern Europe
Czech Republic 1 10.5 100 3,540 8.7 8.4 9 3,484 6.4 6.2 6.7 1.3
Slovakiaa1 5.4 100 795 7.6 7.1 8.2 812 6.0 5.5 6.5 1.3
Poland 5 11.9 31.2 2,334 5.7 5.5 6 2,201 4.0 3.9 4.3 1.4
Belarus 1 9.5 100 1,564 5.5 5.3 5.8 1,716 3.9 3.7 4.1 1.4
Bulgariaa1 7.5 100 1,398 5.0 4.8 5.3 1,311 3.7 3.5 4.0 1.3
Russian Federation 4 8.6 6.0 1,259 5.1 4.8 5.4 1,326 3.5 3.4 3.8 1.4

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Assessments of the causal association between HIV and
NHL at the global level through ecologic analyses are sub-
ject to well-known biases and any interpretation should be
undertaken with caution. The observation that countries
with a low prevalence of HIV in 2010 had quite variable
NHL incidence rates may relate to the poorer survival of
HIV-infected patients in LMIC, and the possibility that
many patients die before they would have developed NHL.
HIV infection plays an important role in the etiology of
NHL, and it has been estimated that around 5–10% of HIV-
infected patients develop lymphomas [27], and thus coun-
tries with a high prevalence of HIV, such as Uganda (7%,
data not shown), and Zimbabwe (15.5%, data not shown),
the incidence of NHL is expected to be elevated, even in the
presence of some misclassification. As NHL is an AIDS-
defining cancer, incidence rates may have declined upon
the introduction of the antiretroviral treatment, notably in
these Sub-Saharan Africa countries that have been among
the most impacted by the HIV epidemic [28, 29].
Globally, we observed some disparities in the temporal
patterns of NHL incidence in different countries. An expla-
nation for the slight increases in incidence in certain Asian
countries including the Republic of Korea, and Japan is not
clear but may be partially linked to better diagnosis and
complete registration, as well as environmental exposures
and lifestyle factors [30]. HBV has been linked to NHL inci-
dence in Korea [31] and an increasing incidence of NHL
observed at older ages, while HBV prevalence is decreas-
ing at younger ages [32]. A high proportion (50–60%) of
adult T-cell leukemia/lymphoma among NHL in Japan [33]
illustrates the importance of HTLV-I infection on NHL
incidence. The high prevalence of HTLV-1 recorded in
Japan, and certain populations in Africa, South America,
and Caribbean [34] may contribute to the observed elevated
M:F rate ratio male:female
a National registry
Table 2 (continued)
Number of
registries
Population
covered in
million
Population
covered (%)
Males Females M:F
Cases ASR 95% CI Cases ASR 95% CI
Ukrainea1 45.8 100 6,142 4.5 4.4 4.6 5,628 2.9 2.8 3.0 1.5
Northern Europe
Denmarka1 5.5 100 3,005 12.9 12.4 13.4 2,339 8.6 8.2 9.0 1.5
United Kingdom 13 62.8 100 92,940 12.4 12.4 12.6 78,908 9.0 8.9 9.1 1.4
Norwaya1 4.9 100 2,447 12.5 12 13.1 1,949 8.9 8.5 9.4 1.4
Ireland 1 4.5 100 1,843 12.1 11.6 12.7 1,541 9.1 8.6 9.6 1.3
Iceland 1 0.3 100 122 10.8 8.8 12.9 92 7.3 5.7 8.9 1.5
Estoniaa1 1.3 100 411 8.9 8.1 9.9 426 5.8 5.2 6.5 1.5
Lithuaniaa1 3.1 100 808 7.5 7 8.1 923 5.3 5 5.8 1.4
Latvia (2010–2012)a1 2.0 100 271 6.8 6 7.8 337 5.3 4.7 6.1 1.3
Southern Europe
Portugal 1 0.2 1.9 86 13.2 10.4 16.1 60 7.6 5.6 9.8 1.7
Italy 36 24.6 41.5 13,692 12.8 12.6 13.1 11,684 8.9 8.7 9.1 1.4
Malta 1 0.4 100 179 11.2 9.5 13.1 198 10.6 9 12.2 1.1
Spain 14 10.3 22.3 4,230 10.3 10 10.7 3,562 7.3 7.1 7.7 1.4
Cyprusa1 0.8 75.4 285 9.6 8.5 10.8 296 8.6 7.6 9.7 1.1
Sloveniaa1 2.0 100 715 7.9 7.3 8.6 711 6.1 5.6 6.7 1.3
Croatiaa1 4.4 100 1,201 7.4 7 7.9 1,201 5.5 5.2 6.0 1.3
Western Europe
Netherlandsa1 16.6 100 8,306 12.2 12 12.5 6,496 8.2 8 8.5 1.5
France 18 11.9 18.3 5,804 12.1 11.8 12.5 4,713 7.8 7.6 8.1 1.5
Belgiuma1 10.8 100 5,338 12.0 11.7 12.4 4,596 8.5 8.3 8.9 1.4
Switzerland 9 4.4 56.2 2,104 11.5 11 12.1 1,767 7.8 7.4 8.3 1.5
Germany 9 53.1 65.3 25,398 10.3 10.2 10.5 21,552 7.0 6.9 7.1 1.5
Austriaa3 8.4 100 3,746 9.1 8.8 9.5 3,405 6.5 6.3 6.8 1.4
Australia/New Zealand
Australiaa9 21.9 100 25,682 15.3 15.1 15.5 19,526 10.3 10.2 10.5 1.5
New Zealand 3 4.4 100 2,112 13.1 12.5 13.7 1,682 9.1 8.7 9.7 1.4

Cancer Causes & Control
1 3
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Australia
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Austria
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Brazil
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Canada
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
China
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Colombia
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Costa Rica
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Croatia
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Denmark
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Ecuador
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Estonia
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
France
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Germany
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
India
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Ireland
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Italy
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Japan
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Lithuania
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Netherlands
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
New Zealand
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Norway
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Philippines
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Poland
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Republic of Korea
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Slovakia
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Slovenia
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Spain
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Switzerland
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Thailand
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,000
1980 1985 1990 1995 2000 2005 2010
Year
Uganda
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,00
0
1980 1985 1990 1995 2000 2005 2010
Year
United Kingdom
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,00
0
1980 1985 1990 1995 2000 2005 2010
Year
USA: Black
1
1.5
2
2.5
3
3.5
4
5
7
10
12
15
20
25
30
35
40
50
60
Age standardized incidence rate per 100,00
0
1980 1985 1990 1995 2000 2005 2010
Year
USA: White
Age-standardised incidence rates per 100000 in males
Age-standardised incidence rates per 100000 in females
Fig. 3 Time trends in non-Hodgkin lymphoma incidence rates (age-standardized rates-world), in males and females 1980–2012 [Source: Cancer
Incidence in Five Continents plus (1980–2012)]

Cancer Causes & Control
1 3
incidence rates of NHL, that are likely modulated by other
factors. Perry etal. [35] found marked differences in the
frequencies of NHL subtypes in developed and develop-
ing regions; for instance, a lower frequency of B-cell NHL
and higher frequency of T- and NK-cell NHL were seen in
developing regions, while a higher frequency of Burkitt lym-
phoma was observed in parts of Central and South America
and Africa.
Our common observation of a rising incidence in North
America, parts of Europe, and Oceania until the 1990s with
a stabilization thereafter is confirmed by other reports.
van Leeuwen etal. [36] reported NHL incidence increas-
ing during the period 1982–1996, with stable trends seen
from 1997 to 2006. In Spain, Marcos-Gragera etal. [37]
found an attenuation in NHL incidence after 1996, that was
hypotheses as partly explained by the decrease in incidence
of AIDS-related lymphomas among young adults and other
factors. Adamson etal. [38] described the trends in inci-
dence of 13 European countries until 2000, observing an
increase in the number of NHL registration in all countries
of the study [38].
While a higher incidence of NHL has been consistently
reported In North America and other developed countries
and one that has been linked to the HIV epidemic [37, 39],
the temporal patterns of NHL, must be interpreted with cau-
tion. The improvements in cancer registration, as well as the
changing classification may have impacted on the observed
patterns over time. The Revised European-American Clas-
sification of lymphoid Neoplasms (REAL) became the basis
for the WHO Classification of Tumours of Haematopoietic
and Lymphoid Tissue when originally published in 2001, and
represented a global consensus on hematopoietic classifica-
tion that likely coincides with some of the period-related
changes in the trends observed in this study.
There are also a number of limitations in our study. The
robustness of the national estimates in GLOBOCAN var-
ies by country depending on the availability of high-quality
incidence and mortality data. International comparisons
based on the observed data from PBCR may be subject to
varying coding practices between the registries included in
the CI5 series and within each institution over time. It is
also important to note that incidence data are derived from
subnational cancer registries in many countries, and some
will be more representative of the national profile and time
trends than others. While the registries included in CI5 are
deemed of high quality by an appointed editorial board,
there remains the need to improve the accuracy of informa-
tion on hematological malignancies as defined in the pathol-
ogy reports abstracted at the PBCR. Not all cancer registries
provide specific morphological diagnosis for a sufficiently
large proportion of cases as to be included in analyses by
histological subgroup. Although such analyses may help
interpreting the results in the areas with high-quality pathol-
ogy services, the definition of subtypes may be subjected to
regional variation.
An important strength of our study is the global coverage
assembled via successive volumes of CI5 spanning 30years,
alongside national estimates for all world areas for the year
(A) (B)
Low HDIMedium HDI
High HDI
Human Development Index
Very high HDI
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0
2
4
6
8
10
12
14
0.1
0.2
0.3
0.4
0.5
0.7
1
2
3
5
7
10
20
30
HIV prevalence
Age standardised (World) incidence rate per 100000
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0
2
4
6
8
10
12
14
0.4
0.5
0.6
0.7
0.8
0.9
Human Development Index
Age standardised (World) incidence rate per 100000
Fig. 4 a Prevalence of HIV among adults aged 15–49 years old
in 2010 (log scale) and age-standardized incidence rates 2018 by
Human Development Index; b age-standardized incidence rates and
Human Development Index (natural scale) by the prevalence of HIV
among adults aged 15–49years. The diameter of the circles is rela-
tive to the magnitude of the HIV prevalence and their color represents
HDI level (Sources: GLOBOCAN 2018, WHO Global Health Obser-
vatory, United Nations Development Programme)

Cancer Causes & Control
1 3
2018 from the GLOBOCAN database that can be inspected
at IARC’s Global Cancer Observatory (http://gco.iarc.fr). In
countries with longstanding cancer registries of high qual-
ity, an age-period-cohort analysis is warranted to determine
more explicitly the role of period effects (linked mainly to
artifact, such as changes in practices affecting all studied age
groups at a given time or time period) versus birth cohort
effects (linked mainly to changes in population-level risk
and the prevalence of the underlying determinants among
successive generations).
Conclusion
The marked differences in contemporary NHL incidence
rates by country and region may be partly linked to contrast-
ing levels of access to care and the availability of diagnostic
services. In addition, endemic infections and environmen-
tal exposures in regions in Africa, Asia, and Latin America
likely contribute to these differences. Changes in classifica-
tion of NHL have been applied at different time points in the
contributing registries, and these may have partially affected
the observed patterns and time trends. All of these factors
need to be taken into account to gain further insight into this
complex set of diseases.
Acknowledgments The work reported here was undertaken by Dr.
Miranda-Filho during the tenure of an IARC Postdoctoral Fellowship,
partially supported by the European Commission FP7 Marie Curie—
Actions—People—co-funding regional, national, and international
programmes (COFUND). We would like to thank the Directors and
staff of the population-based cancer registries worldwide who compiled
and submitted their data for the CI5 and GLOBOCAN projects used
in this paper.
Compliance with ethical standards
Conflict of interest The authors declare no competing interests.
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