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Annals of Oncology
Annals of Oncology 23: 2748–2755, 2012
doi:10.1093/annonc/mds079
Published online 2 May 2012
Geographic distribution of hematopoietic cancers in
the Nile delta of Egypt
C. M. Herzog1†, S. Dey2†, A. Hablas3, H. M. Khaled4, I. A. Seifeldin3, M. Ramadan3,
H. El-Hamzawy3, M. L. Wilson1 & A. S. Soliman1*
1
Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, USA; 2Indian Institute of Public Health, Delhi, Public Health Foundation of India,
New Delhi, India; 3Gharbiah Cancer Registry and Tanta Cancer Center, Tanta, Egypt; 4National Cancer Institute, Cairo University, Cairo, Egypt
Received 29 November 2011; revised 9 February 2012; accepted 13 February 2012
Background: Previous evidence indicated that incidence rates of non-Hodgkin’s lymphoma (NHL) are high in Egypt
although little is known about risk factors.
Materials and methods: Using data from the population-based cancer registry of Gharbiah governorate in Egypt,
we assessed the 1999–2005 incidence of hematopoietic cancers (HCs) based on the ICD-O3 by age- and sex-specific
urban–rural distribution.
Results: NHL showed the highest incidence among all HCs (11.7 per 100 000). Urban incidence of HCs was higher
than rural incidence. Incidence rates of Hodgkin’s lymphoma (HL) and NHL were high especially among urban males
up to the 64-year age category. Rural incidence of HL and NHL was high below age 20. Among the districts of the
governorate, we observed NHL incidence pattern similar to that observed for hepatocellular carcinoma because of the
possible link to hepatitis C virus for both cancers. Comparison to the published HCs data from Algeria, Cyprus, and
Jordan showed the highest NHL rate in Egypt than the other countries in the region.
Conclusions: Future studies should define the role of environmental exposures in hematopoietic carcinogenesis in
this population. In-depth studies should also investigate the role of access to health care in the urban–rural variation of
HC distribution in this population.
Key words: Egypt, hematopoietic cancer, Hodgkin’s lymphoma, incidence, non-Hodgkin’s lymphoma
introduction
Hematopoietic cancers (HCs) are diverse groups of diseases
including leukemias, lymphomas, plasma cell tumors,
myelodysplastic syndromes, and mastocytosis. They arise
primarily from two categories of immunological cell types—
myeloid and lymphoid cells [1]. Tumors involving the
lymphoid group are more common and the classification
between lymphomas and leukemias has become blurred over
the last few years [1]. Among lymphomas, Hodgkin’s
lymphoma (HL) has low incidence rates across the world with
small variations. In the United States, the incidence of HL is
∼3 per 100 000, while it is <1 per 100 000 in parts of Asia and
sub-Saharan Africa [2]. Non-Hodgkin’s lymphoma (NHL)
though has much higher global incidence than HL with wider
variations across the world [3]. Most developed countries as
well as West Asia report rates of NHL >10 per 100 000, while
*Correspondence to: Dr A. S. Soliman, Department of Epidemiology, University of
Michigan School of Public Health, 5626 SPH I 1415 Washington Heights, Ann Arbor, MI
48109-2029, USA. Tel: +1-734-764-5469; Fax: +1-734-764-3192; E-mail: asoliman@
umich.edu
†
Equal first-authorship.
parts of South and East Asia and Africa report rates of <5 per
100 000 [2]. Incidence rates of leukemia are intermediate in the
East Mediterranean region between lowest rates in Africa, e.g.
Uganda’s incidence rate of 1.3 per 100 000 in males and 1.4
per 100 000 in females and highest incidence rates in New
Zealand (14.8 per 100 000 in males and 8.7 per 100 000 in
females) [4, 5].
Among developing countries, the incidence of HC is low
with Egypt being one of the exceptions. Egypt has one of the
highest incidence rates of lymphoma in the world, mainly
NHL, which is higher than even the United States [4, 5] as well
as other developed nations where HCs are more common. In
Egypt, NHL is the second most common cancer in adults and
lymphoma is the most common cancer in children [6].
Previous studies of HC have been carried out in Egypt, but
they mostly contain data from pathology-based laboratories [7]
or localized registries from predominantly urban areas with
limited variations in risk factors and exposures [8]. As a part of
this study, we explored patterns of incidence of HCs in the
Gharbiah governorate, situated in the center of the Nile Delta
Region (NDR) of Egypt, from the country’s only populationbased cancer registry. This study capitalized on the unique
opportunities to investigate HC in this region since our
© The Author 2012. Published by Oxford University Press on behalf of the European Society for Medical Oncology.
All rights reserved. For permissions, please email: [email protected].
original articles
Annals of Oncology
previous studies from NDR have depicted distinct variations in
environmental and occupational exposures [9–12], variations
based on urban and rural residence [13–15], and distribution
of possible risk factors for HC [15–19].
materials and methods
The Gharbiah population-based cancer registry (GPCR) was created in
1998 as a part of the Middle East Cancer Consortium (MECC) with
funding from the National Cancer Institute in Bethesda and is located in
Tanta, the capital of Gharbiah Governorate [6]. The active registry also
collects information on cancer patients who reside in Gharbiah but are
diagnosed in neighboring governorates. Methods for ensuring data quality,
eliminating duplication, and information on registry staff training and
experience have been documented previously [15, 16].
study population
The case definition for the study population consisted of all patients in the
GPCR diagnosed with any hematopoietic malignancy (ICD-O3
morphology codes 9590-9989) between the years 1999 and 2005. The
following variables were obtained for each case: registry number, sex, birth
date, age at diagnosis, address, region, marital status, smoking status,
occupation, family history, date, place and basis of diagnosis, topography,
morphology, laterality, grade, stage, follow-up and cause of death
information, medical record number, treatment, and place of reference.
Missing values and inconsistencies in these variables were addressed by
examining medical records and not considered in further analysis, if
unresolved. While not all cases were deceased, it was not within the scope
of this study to independently acquire additional risk factor information or
supplement missing values through interviews. Use of human subject data
was approved by the University of Michigan Institutional Review Board
and the Gharbiah Cancer Society Research Ethics Committee.
The Gharbiah governorate consists of eight districts, each with its own
main city of the same name while the rest of the districts are rural with a
total of 316 villages in the governorate. According to the recent 2006
Central Agency for Public Mobilization and Statistics (CAPMAS) census
[20], Gharbiah has a population of slightly > 4 million (49% female, 51%
male). Approximately 30% of the population resides in urban areas with
∼52% of the population below the age of 24 and 3.8% above the age of 65.
Census data for Gharbiah governorate were obtained from the 1996,
2006, and 2011 census reports of CAPMAS [20]. A constant linear growth
of the population was assumed to project populations in the intervening
years. At the district level, the census data consisted of 16 age categories
(5-year intervals). Pediatric cases were defined as <15 years of age, whereas
adults were defined as 15 years of age and above. These population figures
formed the denominators to calculate the overall, age-specific, districtspecific, and urban–rural incidence rates for hematopoietic malignancies.
The urban–rural classification followed the CAPMAS coding of urban
and rural areas. Urban areas consisted of the capital cities of the eight
districts of the Gharbiah governorate, while the remaining areas in the
governorate were considered rural. Each case in the registry is assigned a
residence code based on their city or village of residence and this code was
used to classify patients as urban or rural.
data management and statistical analysis
Nodal lymphomas included those tumors arising in lymph nodes,
Waldeyer’s ring, the tonsils, and the spleen. All other topologies were
considered extranodal lymphomas [21]. Aggressiveness of NHL tumors was
assessed similar to the REAL classification system [22].
Volume 23 | No. 10 | October 2012
For comparability to other data, the subtypes were grouped using the
World Health Organization (WHO) classification according to the
HAEMACARE project classification [23].
Annual and average age- and sex-specific incidence rates for the period
1999–2005 were calculated using the number of hematopoietic malignancy
cases as the numerator and the corresponding age- and sex-specific
population data from CAPMAS as the denominator. Univariate analyses
were carried out with demographic indicators and other registry variables
to better understand the characteristics of the study population.
Interannual variation in the number of cases was examined using χ2
testing. Incidence rate ratios (IRRs) were calculated and used when
comparing the eight districts to each other. Additionally rates were
calculated to compare urban and rural regions in Gharbiah. Direct ageadjusted incidence rates were calculated by direct age standardization for
the districts and Gharbiah using WHO’s world standard population [2].
These rates were then compared with data of the registries of Algeria,
Cyprus, and Jordan published in the MECC monograph, Cancer Incidence
in Five Continents version IX and GlobalCan [4, 5, 24]. All statistical
operations were carried out in SAS 9.2 (SAS Institute, Cary, NC).
results
There were 4288 cases (58.6% male, 41.4% female) of HCs in
GPCR from the years 1999–2005 (Table 1). Most of the cases
were rural (58.2%) and belonged to the district of Tanta
(29.6%) followed by the district of El-Mehalla (22.2%).
Approximately half the lymphoma cases had presented in later
stages of the disease (54%) and had been diagnosed by the
histology of the primary tumor (85.9%). The majority of the
lymphomas were nodal (73.5%) and were moderately
aggressive (49.9%) (Table 1).
Table 2 depicts the crude age-specific as well as age-specific
incidence rates of the major groups of HCs compared by
urban–rural status residence of cases. Crude rates showed
higher incidence for all HL, NHL, and leukemia in males than
females, except for HL in the age group of 65–74, and
leukemia in the age-group of 50–64, where females had higher
incidence rates than males. In addition, incidence rates of all
three malignancies showed steady increase with aging
(Table 2). Overall age-standardized incidence rates of
lymphomas and leukemias were higher among males than
females in both urban and rural populations. Also, urban
incidence was higher than rural incidence when comparing
overall incidence rates with most age-specific incidence rates.
The maximum urban–rural differences were observed for
urban incidence of leukemia (IRR = 4.89; 95% CI = 1.53–15.59)
and HL (IRR = 3.91; 95% CI = 0.35–43.15) in the 75+ age
category. Distribution of incidence of HCs by districts of
Gharbiah (Figure 1) depicted highest incidence rates in the
central districts of Kotour and Tanta.
Supplemental Table S1 (available at Annals of Oncology
online) and Table 3 present the crude incidence rates for
lymphoid and myeloid malignancies in the Gharbiah registry
by age and morphologic types based on the WHO and
HEMACARE classification [23]. ‘Diffuse B-cell lymphoma’,
‘malignant lymphoma, large B-cell diffuse NOS’, ‘malignant
lymphoma, small B-cell lymphocytic’, and ‘B-cell chronic
lymphocytic leukemia/small lymphocytic lymphoma’ were the
most common types among the mature B-cell neoplasms.
doi:10.1093/annonc/mds079 | 
original articles
Annals of Oncology
Table 1. Characteristics of the study population and patterns of
hematopoietic cancers in Gharbiah, Egypt (1999–2005)
Variable
Total cases
Sex
Residence
Year of diagnosis
Districts
Stage of cancera
Basis of diagnosis
Tumor site(3081)c
Aggressiveness of
tumor(2462)c
Descriptive category
Male
Female
Urban
Rural
1999
2000
2001
2002
2003
2004
2005
Tanta
El-Mehalla
Kafr El Zayat
Zefta
Samanood
Santa
Kotour
Basyoon
Localized (I)
Regional (Dir. Ext; Ext. LN; and
NOS, II)
Distant (III, IV)
Unknown
Histology of primary
Cytology/hematology
Clinical/Ult./X-ray
Death certificate only
Otherb
Nodal
Extranodal
Indolent
Aggressive
Highly aggressive
Total
No.
Cases
(%)
4288
2511
1777
1793
2495
577
585
601
588
643
645
649
1269
952
437
365
202
377
381
305
536
824
100.0
58.6
41.4
41.8
58.2
13.5
13.6
14.0
13.7
15.0
15.0
15.1
29.6
22.2
10.2
8.5
4.7
8.8
8.9
7.1
12.5
19.2
2315
613
3683
261
110
204
30
1759
635
745
1229
488
54.0
14.3
85.9
6.1
2.6
4.8
0.7
73.5
26.5
30.3
49.9
19.8
a
Stage of cancer was defined according to the SEER Summary Staging
Manual, 2000. Stages of cancer were categorized as: localized: stage I
lymphoma and solitary plasmacytoma; regional, NOS: stage II lymphoma;
distant: stage III and IV lymphoma as well as all leukemia, multiple
myeloma, and myelodysplastic syndrome.
b
Other includes: clinical only, exploratory surgery/autopsy, specific
biochemical/immunological test, and histology of metastases.
c
Lymph node involvement and aggressive nature were assessed for
lymphomas only, with sample sizes of 2394 and 2462, respectively. Dir.ext.,
direct extension; Ext. LN, extranodal lymph node; NOS, not otherwise
specified; Ult., ultrasound.
Among the HL, mixed cellularity was the most common type
in this group (supplemental Table S1, available at Annals of
Oncology online). Among the myeloproliferative neoplasms,
chronic myelocytic leukemia was the most common type
(Table 3).
When categorized by clinical types, the incidence of NHL
was the highest (11.7 per 100 000) followed by leukemia (5.30
per 100 000) and HL (1.72 per 100 000) (supplemental
 | Herzog et al.
Table S2, available at Annals of Oncology online). When the
rates of HL, NHL, and leukemia of Egypt were compared with
the rates of countries from the Middle Eastern region (Algeria,
Cyprus, and Jordan) [4, 5, 24], Egypt showed the highest
incidence of NHL than other Middle Eastern countries
(supplemental Table S2, available at Annals of Oncology
online).
On analyzing the extent of involvement of nodal sites with
regards to lymphoma, apart from lymph nodes of multiple
regions (C77.8) (43.9%), the maximum involvement was of
lymph nodes of head and neck (C77.0) (14.0%) followed by
abdominal lymph nodes (C77.2) (12.4%). Among the
extranodal sites, maximum involvement was seen for
gastrointestinal tract (GIT) (29.7%) followed by head and neck
(20.0%). The top five primary sites for extranodal lymphoma
were stomach (C16) (15.4%), bone (C40-41) (12.9%), soft
tissue (C49) (11.0%), skin (C44) (9.4%), and nasopharynx
(C11) (8.7%).
discussion
This study is the largest and only population-based study on
HCs from Egypt. The study has five interesting observations.
First, we observed a higher urban than rural incidence of HCs
with a maximum difference for leukemia and HL in the 75+
age category. Second, we identified a regional variation of HCs
among the districts with highest rates seen for central districts
followed by the western districts and the lowest rates in the
most eastern districts. Third, NHL was the most common
malignancy with diffuse B-cell neoplasms being the most
common type of NHL. Chronic lymphocytic leukemia was the
most common subtype of leukemia. Fourth, the most common
extranodal sites were GIT, head and neck, and bone. Fifth,
there were international variations of HCs when the Egyptian
rates were compared with the rates of neighboring countries.
Incidence of NHL in Egyptians was higher than the incidence
in Algeria, Cyprus, and Jordan, but the incidences of HL and
leukemia in Egypt were intermediate compared with the
incidences of these two HC types in Algeria, Jordan, and
Cyprus [4, 5, 25].
In this study, we observed a higher urban incidence for all
HCs albeit the differences in urban and rural incidence
were <100%; we did see an approximately four times higher
incidence of leukemia and HL among the 75+ year urban
males. We do not believe that there is a significant difference in
access to primary health care between rural and urban regions
in our study population. Egypt has one of the best coverage of
primary health care systems in the world through rural health
units and urban health centers [25]. However, complete
unbiased ascertainment and accurate diagnosis of different
subtypes of HC are challenging even in developed countries
[26]. In addition, socioeconomic factors did not show to be a
factor in HC subtype differences in developed countries [27].
However, variation of health care access and detailed case
ascertainment are worthy of future thorough investigations in
developing countries like Egypt.
NHL has a similar risk profile with higher occurrence seen
in immune-suppressed individuals or individuals infected with
hepatitis C virus (HCV), Epstein–Barr virus, or HIV [28, 29].
Volume 23 | No. 10 | October 2012
original articles
Annals of Oncology
Table 2. Crude and age-standardizeda incidence rates (100 000) by sex, overall, and by urban–rural status for Hodgkin’s lymphoma, non-Hodgkin’s
lymphoma, and leukemia in Gharbiah, Egypt
Cancer site
Gharbiah overall
IRb
Male
Female
Hodgkin’s lymphoma (C81)
<20
1.96
0.91
20–49
2.46
1.11
50–64
2.84
2.05
65–74
2.19
2.40
75+
2.58
0.74
Total
2.28
1.15
Non-Hodgkin’s lymphoma (C82–C85, C96)
<20
2.58
1.31
20–49
10.12
6.35
50–64
38.11
32.55
65–74
61.57
48.20
75+
60.25
52.57
Total
11.45
8.42
Leukemia (C91–95)
<20
3.53
2.27
20–49
3.10
2.90
50–64
7.71
7.80
65–74
9.30
8.79
75+
12.05
11.11
Total
4.00
3.36
Gharbiah overall
IRa
Male
Female
Gharbiah urban
IRa
Male
Female
Gharbiah rural
IRa
Male
Female
Urban–rural IRR (95% CI)b
Male
Female
0.79
0.99
0.37
0.11
0.05
2.30
0.36
0.45
0.27
0.12
0.01
1.21
1.13
1.55
0.48
0.12
0.10
3.37
0.58
0.58
0.26
0.13
0.00
1.56
0.65
0.74
0.31
0.11
0.03
1.83
0.28
0.38
0.27
0.11
0.02
1.07
1.72 (1.19–2.50)
2.10 (1.51–2.93)
1.55 (0.82–2.92)
1.11 (0.27–4.66)
3.91 (0.35–43.15)
1.84 (1.47–2.31)
2.09 (1.20–3.62)
1.51 (0.92–2.50)
0.96 (0.43–2.16)
1.18 (0.29–4.71)
0.00
1.46 (1.05–2.02)
1.03
4.05
4.95
3.08
1.21
14.32
0.52
2.54
4.23
2.41
1.05
10.75
1.37
5.37
6.06
3.67
1.63
18.10
0.53
3.30
5.11
3.93
1.44
14.31
0.90
3.47
4.31
2.76
0.99
12.43
0.52
2.19
3.75
1.76
0.90
9.12
1.52 (1.10–2.12)
1.55 (1.31–1.83)
1.40 (1.18–1.67)
1.33 (1.02–1.73)
1.65 (1.03–2.64)
1.46 (1.32–1.61)
1.03 (0.62–1.70)
1.51 (1.23–1.87)
1.36 (1.12–1.65)
2.23 (1.67–2.98)
1.59 (0.99–2.57)
1.57 (1.39–1.77)
1.41
1.24
1.00
0.47
0.24
4.36
0.91
1.16
1.01
0.44
0.22
3.74
1.79
1.34
1.19
0.70
0.51
5.53
1.27
1.47
1.27
0.71
0.21
4.94
1.27
1.19
0.89
0.34
0.10
3.80
0.77
1.02
0.87
0.32
0.23
3.20
1.41 (1.06–1.87)
1.12 (0.82–1.54)
1.33 (0.90–1.97)
2.09 (1.06–4.09)
4.89 (1.53–15.59)
1.46 (1.22–1.73)
1.65 (1.16–2.35)
1.45 (1.06–1.98)
1.45 (0.98–2.16)
2.22 (1.12–4.39)
0.94 (0.30–2.96)
1.54 (1.27–1.86)
a
Age-standardized to the world population.
Crude rate.
CI, confidence interval; IR, incidence; IRR, incidence rate ratio.
b
There is also limited evidence suggesting association of NHL
with higher exposure to ultraviolet light [30] and pesticides
[31]. Ionizing radiation and alkylating agents such as those
used for chemotherapy have been investigated in relation to
HC [32–37]. However, none of the studies that investigated
these exposures in relation to HC were conducted in Egypt or
other African countries.
Prevalence of HCV infection is ∼13.9% of the healthy
population with higher rates of up to 15.8% in Northern Egypt,
including Gharbiah [38]. Such a high rate of HCV infection is
related to the increasing incidence of hepatocellular cancer
(HCC) in Egypt [16] while at the same time is also probably
responsible for the high rates of NHL, especially B-cell type
NHL, observed in our present study. The common role of
HCV infections for HCC and NHL is also supported by the
pattern of incidence of HCs in the districts of Gharbiah
(Figure 1) which is mainly driven by NHL and is quite similar
to that seen for HCC [16]. HCV infection has also been linked
to increased risk of B-cell NHL [39] and to diffuse large B-cell
marginal zone and follicular lymphoma in studies from the
National Cancer Institute of Cairo University in Egypt [40].
The role of HCV infection in NHL is further strengthened by
immunohistochemical studies that detected HCV RNA in
malignant NHL tissues from Egypt [41]. A recent report of
cancer incidence in Aswan in South Egypt showed a
significantly lower rate of NHL (crude rate of 1.9 per 100 000
and age-standardized rate of 1.9 per 100 000) than the rate
Volume 23 | No. 10 | October 2012
reported from Gharbiah in this study [42]. However, the rates
of HL and leukemia in Aswan were not significantly different
from the rates in Gharbiah (1.2 per 100 000 and 1.3 per
100 000, crude and adjusted rates, respectively, for HL and 5.3
per 100 000 and 6.6 per 100 000, crude and adjusted rates,
respectively, for leukemia in Aswan). Higher rates of NHL in
Gharbiah than South Egypt and other neighboring countries
are likely due to the higher infection rate of HCV in Gharbiah
than in South Egypt and the Middle East [43].
HCV has been attributed as a causal role in NHL in the past
and there are putative reasons to support this from a large
number of epidemiological studies with estimates suggesting a
two to four times higher risk of NHL occurrence among HCVpositive individuals [43, 44]. HCV infection mainly affects B
cells resulting in a benign lymphoproliferation and mixed
cryoglobulinemia [45, 46]. The association of HCV infection
and NHL is clear in Egypt since the pattern of incidence of
lymphomas is quite similar to the pattern of incidence of HCC
(which can be considered a proxy for HCV infection) in the
districts of Gharbiah [16]. Unfortunately, there are no available
results on the exact infection rate of HCV among the
population of the Gharbiah governorate.
Smoking has been linked to HC but the associations have
been either weak or nonexistent. For example, weak-positive
association was observed for cigarette smoking and HL [47]
and for follicular but not other types of NHL [48]. Other
studies showed no excess risk of NHL with tobacco smoking
doi:10.1093/annonc/mds079 | 
original articles
Annals of Oncology
Table 3. Number of cases and crude incidence rate (IR) per 100 000 for myeloid malignancies diagnosed in Gharbiah 1999–2005 by sex and morphologic
type
HAEMACARE groupings
Acute myeloid leukemia
Subgroup 1
Subgroup 2
Subgroup 3
Subgroup 4
Myeloproliferative neoplasms
CML
Other myeloproliferative neoplasms
Subgroup 1
Subgroup 2
Myelodysplastic syndrome
ICD-O-3
code
ICD-O-3 description
9840
9861
9867
9870
9872
9873
9874
9891
9910
9930
9866
Acute erythroid leukemia
AML, NOS
Acute myelomonocytic leukemia
Acute basophilic leukemia
AML, minimal differentiation
AML without maturation
AML with maturation
Acute monocytic leukemia
Acute megakaryoblastic leukemia
Myeloid sarcoma
Acute promyelocytic leukemia t(15; 17) (q22; q1112)
AML with abnormal marrow eosinophils
AML, t(8,21) (q22,q22)
AML, 11q23 abnormalities
AML, with multilineage dysplasia
Refractory anemia with excess blasts in
transformation (obsolete)
Acute panmyelosis with myelofibrosis
9871
9896
9897
9895
9984
9931
266
0
71
23
1
8
36
65
22
3
1
30
1.03 140
0
0
0.27 37
0.09
9
0.00
1
0.03
6
0.14 20
0.25 38
0.09 10
0.01
1
0.00
0
0.12 16
1.07 126
0
0
0.28 34
0.07 14
0.01
0
0.05
2
0.15 16
0.29 27
0.08 12
0.01
2
0.00
1
0.12 14
0.99
0
0.27
0.11
0
0.02
0.13
0.21
0.09
0.02
0.01
0.11
0.00
0.00
0
0.01
0
0
0.00
0
0.01
0
1
1
0
1
0
0.01
0.01
0
0.01
0
1
1
0
2
0
Males
No. of
cases
0
0
0
1
0
IR
Females
No. of
cases
IR
0.01
1
0.85 103
0.78 95
0.02
1
0
0
0.01
2
0.03
2
0
1
0.01
2
0
0
0
0
0.14 16
0.07
8
0
0
0.03
3
0
0
0
0
0.03
5
0.02
2
0.01
1
0.79 117
0.72 106
0.01
5
0
0
0.02
1
0.02
5
0.01
0
0.02
0
0
0
0
0
0.12 20
0.06 11
0
0
0.02
6
0
0
0
0
0.04
3
0.02
3
0.01
0.92
0.83
0.04
0
0.01
0.04
0
0
0
0
0.16
0.09
0
0.05
0
0
0.02
0.02
9945
9876
9946
9975
Chronic myelomonocytic leukemia
Atypical CML, BCR/ABL-1 negative
Juvenile myelomonocytic leukemia
Myelodysplastic/myeloproliferative
9800
9801
9805
9806
Leukemia, NOS
Acute leukemia, NOS
Acute leukemia, ambiguous lineage
Myeloid leukemia, NOS
0.02
2
0
0
0
0
0
0
0.77 119
0.66 99
0.10 20
0
0
0
0
2.80 380
0.02
2
0
0
0
1
0
0
0.91 79
0.75 73
0.15
6
0
0
0
0
2.90 345
0.02
0
0.01
0
0.62
0.57
0.05
0
0
2.70
9863
9875
9950
9961
9962
9963
9964
9960
Myelodysplastic/myeloproliferative
neoplasms
Myeloid leukemia, NOS
All myeloid malignancies
IR
2
220
CML, NOS
201
Chronic myelogenous leukemia, BCR/ABL positive
6
0
Polycythemia vera
3
Myelosclerosis with myeloid metaplasia
7
Essential thrombocythemia
1
Chronic neutrophilic leukemia
2
Hypereosinophilic syndrome
0
Chronic myeloproliferative disease, NOS
0
36
Refractory anemia
19
Refractory anemia with sideroblasts
0
Refractory anemia with excess blasts
9
Refractory cytopenia with multilineage dysplasia
0
Myelodysplastic syndrome 5q deletion
0
Myelodysplastic syndrome, NOS
8
5
9980
9982
9983
9985
9986
9989
Unknown myeloid neoplasms
Leukemia, NOS
Total
No. of
cases
4
0
1
0
198
172
26
0
0
725
AML, acute myeloid leukemia; NOS, not otherwise specified; CML, chronic myeloid leukemia.
[49–52] with other exceptions [53–55]. Rates of smoking are
high and increasing in Egypt [56, 57] but smoking has not
been studied in relation to HC.
 | Herzog et al.
The majority of lymphomas in our study were nodal and
the proportion was consistent with the values seen in the
United States where two-thirds of lymphoid malignancies
Volume 23 | No. 10 | October 2012
original articles
Annals of Oncology
Figure 1. Crude incidence rates for hematopoietic cancers in the eight districts of Gharbiah, 1999-2005 (Map from Lehman et al., 2008 [16]).
arise in the lymph nodes, while only one-third arise in
extranodal sites [1]. However, among the extranodal sites, it
was interesting to note that gastrointestinal and head and
neck sites were the most commonly involved sites. It is
important to note that the rate of extranodal lymphoma in
our study (26.5%) is significantly higher than the extranodal
rates reported in recent studies from Iran (11.5%) and Korea
(12.4%) [58, 59].
Our study had a number of strengths, chief among which
was the fact that this was the first study on HCs from Egypt
from a population-based registry. The population in this region
of Egypt is quite stable with low migration rates [20] and as
such our estimates on the geographical variations of incidence
rates were quite valid. However, our study also had inherent
shortcomings of registry data, in general, with respect to lack of
detailed information on the distribution of risk factors among
individual cases.
In conclusion, this study showed urban–rural as well as
district-level geographical differences of the types of
hematopoietic malignancies in the NDR of Egypt. The study
highlights the geographical distribution for both NHL and
HCC in the study region and the possible parallel link between
HCV and both cancers. Future detailed studies at the
individual level in this population should consider the possible,
unique infections, lifestyle factors and environmental risk
factors, especially for NHL.
funding
CMH was supported by the Cancer Epidemiology Education in
Special PopulationsProgram of the University of Michigan
through funding from the National Institutes of Health (R25
CA112383).
Volume 23 | No. 10 | October 2012
disclosure
The authors do not have conflict of interest or funding sources
that might generate a conflict of interest.
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Annals of Oncology 23: 2755–2762, 2012
doi:10.1093/annonc/mds069
Published online 6 April 2012
Trends in cancer mortality in China: an update
P. Guo1, Z. L. Huang2, P. Yu1 & K. Li1*
1
Department of Preventive Medicine; 2Department of Laboratory of Cell Senescence, Shantou University Medical College, Shantou, China
Received 5 January 2012; revised 7 February 2012; accepted 8 February 2012
Background: Cancer deaths of China with the world population nearly a quarter will have a severe impact on global
cancer trend and burden. The study aims to provide a comprehensive overview of long-term trends in cancer mortality
in China.
Materials and methods: We used joinpoint analysis to detect changes in trends and generalized additive models to
study birth cohort effect of risk factors between 1987 and 2009.
Results: Mortality of all cancers declined steadily in urban areas, but not in rural areas. Decreasing mortality from
cancers of the stomach, esophagus, nasopharynx, and cervix uteri was observed, while lung and female breast cancer
mortality increased. Mortality from leukemia remained relatively stable, and cancer of liver, colorectal, and bladder had
different trends between the rural and urban areas. Generational risks peaked in the cohorts born around 1925–1930
and tended to decline in successive cohorts for most cancers except for leukemia, whose relative risks were rising in
the very recent cohorts.
Conclusion: The observed trends primarily reflect dramatic changes in socioeconomic development and lifestyle in
China over the past two decades, and mortality from cancers of lung and female breast still represents a major public
health priority for the government.
Key words: birth cohort, cancer, China, mortality, trend
introduction
Cancer is a major burden globally that continues to increase
largely due to aging, population growth, and an increasing
adoption of cancer-causing behavior [1]. Official data from
China indicated that cancer had become the second most
common cause of death in China during 2004–2005 [2]. The
age-standardized mortality rate of cancer was 135.88 per
million, accounting for 22.3% of the total deaths [2]. However,
*Correspondence to: Dr K. Li, Department of Preventive Medicine, Shantou University
Medical College, No. 22 Xinling Road, Shantou, Guangdong 515041, China.
Tel: + 0086-754-88-90-04-45; Fax: + 0086-754-88-55-75-62; E-mail: [email protected]
the level of cancer mortality rates differed markedly between
the sexes, as well as the areas in China [3–5].
Previous studies reported the incidence and mortality trends
of selected cancers for limited Chinese populations and time
periods [6–9] and also for some specific cancers in high-risk
areas [10–12]. Although Chinese data of cancer mortality on a
national scale over the period of 1987–1999 had been reviewed
in a previous report [13], China has undergone many changes
over the past decade. Therefore, an up-to-date evaluation of
cancer trends is warranted.
It is presently impossible to obtain the national population
incidence; however, mortality is used in this study. Previous
studies predominantly analyzed the temporal trends in cancer
© The Author 2012. Published by Oxford University Press on behalf of the European Society for Medical Oncology.
All rights reserved. For permissions, please email: [email protected].