Epidemiological and Sociodemographic Transitions of Female Bre - 2022 - Journal

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Journal of Advanced Research 37 (2022) 185–196

Contents lists available at ScienceDirect

Journal of Advanced Research


journal homepage: www.elsevier.com/locate/jare

Epidemiological and sociodemographic transitions of female breast


cancer incidence, death, case fatality and DALYs in 21 world regions and
globally, from 1990 to 2017: An Age-Period-Cohort Analysis
Sumaira Mubarik a, Yong Yu b, Fang Wang a, Saima Shakil Malik c, Xiaoxue Liu a, Muhammad Fawad d,e,
Fang Shi a, Chuanhua Yu a,f,⇑
a
Department of Epidemiology and Biostatistics, School of Health Sciences, Wuhan University, Wuhan 430071, China
b
School of Public Health and Management, Hubei University of Medicine, 30# South Renmin Road, Shiyan, Hubei 442000, China
c
Department of Genetics, The University of Alabama at Birmingham, Birmingham, AL 35294, USA
d
Zhengzhou Key Laboratory of Big Data Analysis and Application, Henan Academy of Big Data, Zhengzhou University, Zhengzhou 450052, China
e
School of Mathematics and Statistics, Zhengzhou University, Zhengzhou 450001, China
f
Global Health Institute, Wuhan University, Wuhan 430071, China

h i g h l i g h t s g r a p h i c a l a b s t r a c t

 Breast cancer (BC) is the most widely


studied disease due to its higher
prevalence, heterogeneity and
mortality.
 Age-standardised rate of BC incidence
was high in high-income North
America, Western Europe and
Australia in 2017. Whereas it was
significantly increased by 89.5%
between 1990 and 2017 in East Asia.
 There was a strong negative
correlation between SDI and case
fatality percent (r2017= 0.93) in 2017
around the globe.
 Substantially high case-fatality-
percent (CFP) was observed in six-
world regions (CFP>40%), and the
highest was in Central Sub-Saharan
Africa (68%).
 Overall, the risk of case-fatality rate
tended to decrease most noticeably in
high middle SDI countries, and the
reduction of the risk of case-fatality
rate in the recent cohort was the
lowest in the low SDI countries.

a r t i c l e i n f o a b s t r a c t

Article history: Introduction: Breast cancer (BC) is the most widely studied disease due to its higher prevalence, hetero-
Received 17 March 2021 geneity and mortality.

Abbreviations: BC, breast cancer; GBD, global burden of diseases; CFR, case-fatality rates; CFP, case-fatality-percent; SDI, sociodemographic index; YLDs, years lived with
disability; YLLs, years of life lost; DALYs, disability adjusted life years; DR, death rates; IR, incidence rates; ASIR, age-standardized incidence rates; ASDR, age-standardized
death rates; APC, age-period-cohort.
Peer review under responsibility of Cairo University.
⇑ Corresponding author at: Department of Epidemiology and Biostatistics, School of Health Sciences, Wuhan University, 185 Donghu Road, Wuhan, Hubei 430071, China.
E-mail addresses: [email protected] (S. Mubarik), [email protected] (C. Yu).

https://doi.org/10.1016/j.jare.2021.07.012
2090-1232/Ó 2022 The Authors. Published by Elsevier B.V. on behalf of Cairo University.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
S. Mubarik, Y. Yu, F. Wang et al. Journal of Advanced Research 37 (2022) 185–196

Revised 24 June 2021 Objectives: This study aimed to compare female BC trends among 21 world regions and globally over
Accepted 29 July 2021 28 year of data and to assess the association between sociodemographic transitions and female BC risks.
Available online 2 August 2021 Methods: We used Global burden of disease study data and measure the female BC burden according to
21 world regions and sociodemographic indices (SDI). Age-period-cohort (APC) analysis was used to esti-
Keywords: mate time and cohort trend of BC in different SDI regions.
Breast cancer Results: By world regions, age-standardised rate of female BC incidence were high in high-income-North
Incidence
America (ASR, 92.9; (95 %UI, 89.2, 96.6)), Western Europe (84.7; (73.4, 97.2)) and Australia (86; (81.7,
Case fatality
90.2)) in 2017. Whereas this rate was significantly increased by 89.5% between 1990 and 2017 in East
World regions
Age-period-cohort Asia. We observed negative association between SDI and death, and DALYs in 25th and below percentiles
of death and DALYs for the worldwide regions. Further, there was observed a strong negative correlation
between SDI and case fatality percent (r2017 = 0.93; r1990 = 0.92) in both 2017 and 1990 worldwide and
highest case fatality percentage was observed in Central Sub-Saharan Africa. Overall, the risk of case-
fatality rate tends to decrease most noticeably in high middle SDI countries, and the reduction of the risk
of case-fatality rate in the recent cohort was the lowest in the low SDI countries.
Conclusions: Remarkable variations exist among various regions in BC burden. There is a need to reduce
the health burden from BC in less developed and under developing countries, because under-developed
countries are facing higher degree of health-related burden. Public health managers should execute more
classified and cost-effective screening and treatment interferences to lessen the deaths caused by BC, pre-
dominantly among middle and low SDI countries having inadequate healthcare supplies.
Ó 2022 The Authors. Published by Elsevier B.V. on behalf of Cairo University. This is an open access article
under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction ations on disease incidence and mortality rate are distinguished in


the APC model. The application of APC methods may facilitate the
Breast cancer (BC) is the most commonly diagnosed cancer assessment of descriptive data, which can be confounded by age,
among women and linked with considerable years of life lost calendar-period, and/or birth-cohort effects. Age effects reflect
(14.9 million DALYs), leading to increased cancer-related morbid- age-associated genetic events and/or carcinogenic exposures. Per-
ity and mortality worldwide [1,2]. The burden of the BC is still iod effects may be observed due to changes in screening practices,
increasing in form of incidence and mortality both in developing diagnostic techniques, or classification definitions. Cohort effects
and developed countries characterizing it as one of the most severe are ‘‘cross-sectional” since they span or cut across all age groups
burdensome cancer worldwide [3,4]. This increasing trend may be and birth-cohorts within a given study period. Birth-cohort effects
an outcome of the obesity epidemic together with dwindling parity are longitudinal because they suggest the net impact of risk factors
[5]. BC incidence rate is higher in high-income countries as com- on the incidence and death rates within one generation or birth
pared to the middle- and low-income ones. Recent literature has cohort [12-14]. Contrasting the rates by regions and age-related
shown that awareness campaigns about BC associated risk factors studies across birth and period cohorts may support in separating
and accessibility to advanced medical treatment have led to signif- functioning of aforementioned factors and expose fluctuations in
icantly decreased BC incidence and mortality rates among high risk patterns that leads toward future etiological findings.
income countries. But still BC incidence is greater in high SDI coun- Various national and regional reports on BC incidence and mor-
tries due to greater population size and lifestyle. However, not only tality have been prepared, but the findings of these multifactorial
the high-income countries are facing BC incidence burden, but it is studies display an inconclusive picture [1,3,7,15]. To the best of
equally devastating to middle- and low-income countries. More- our knowledge no research has been done in context, to compare
over, changes in reproduction pattern, improper awareness along the age period cohort trends among SDI regions and has address
with delayed disease diagnosis and treatment may contributes to effects of socioeconomic development on BC variations during
low incidence among middle- and low-income countries [2,6]. the present study period. Our study not only extend the current lit-
Regardless of advances in medical science, BC is still diagnosed erature on application of APC model on differently regional popu-
in the advanced stages in the countries with inadequate resources lation data but also provide the current statistics of BC in world
as early detection, diagnosis, and proper treatment cannot be pro- regions and globally.
ficiently endorsed. Overall, the 5-year survival rate in BC has been
improved in high-income countries (79%) as compared to middle-
and low-income ones (57%) possibly due to logistical and econom- Materials and methods
ical constraints [7,8]. Clinicians suggested that overall BC survival
can be improved by focusing these four major domains including Data source
cancer recurrence and development of new cancers, late and
long–term disease effects, coordination of care and modifiable The Global Burden of Diseases (GBD) is the most complete sys-
health performances [9]. Moreover, molecular profiling, improved tematic epidemiological study in the world to date. It provides a
drugs and personalized medicine is another emerging area to cure thorough assessment of 359 injuries and diseases, 84 risk factors
the disease with better survival outcomes [10,11]. and 282 reported reasons of death among hundred and ninety-
Studying regional variations related to spatial–temporal trends five countries, twenty-one regions, and seven super-regions. The
in BC (incidence, mortality and DALYs) can be helpful in identifying GBD presents the 2017 estimates and updates for 1990–2016 data
the background factors contributing to these variations and can via innovative estimation methodologies and supplementary
provide indication based and regional intervention of public health sources mentioned in previous studies [16-19]. Information on
policy. In this regard, the age period cohort (APC) model is a com- BC has collected from the Global Health Data Exchange (GHDx)
mon sociological, demographic, and epidemiological model used to online data collection tool (http://ghdx.healthdata.org/gbd-
assess the age, period, and cohort effects independently on disease results-tool). All the details about data sources were defined in
incidence and mortality rate. The three different time related vari- ‘‘Availability of data and materials” statement at end of the article.
186
S. Mubarik, Y. Yu, F. Wang et al. Journal of Advanced Research 37 (2022) 185–196

Data on BC were collected from 1990 to 2017 on the annual inci- the principal approach for estimation on prevalence and incidence
dence, death, disability adjusted life years (DALYs), and age stan- of 354 injuries and diseases in 195 countries and territories. BC
dardized rate (ASR, per 100 k). The sociodemographic index (SDI) mortality data from vital registration systems and mortality pro-
was built to categorize countries into five quintiles (high SDI, high jections were used as input data into CODEm (Death Ensemble
middle SDI, middle SDI, low middle SDI, low SDI) based on national Model) [21]. The CODEm estimates mortality based on available
per capita income, average years of education among persons data and covariates, including education, SD1, smoking, lagging
above 15 years of age and total fertility rate. This index ranges from distribution income, and alcohol consumption. Using the CodCor-
0 to 1 i.e., least to most developed ones. Further, SDI classification, rect procedure, the single cause estimates have been modified to
distribution and list of countries has added as supplemental file. fit all-cause mortality calculated separately [22,23]. Years lived
According to GBD study, BC incidence estimates based on indi- with disability (YLDs) were determined by multiplying the preva-
vidual cancer registries or integrated cancer registry databases. lence of each sequela by its weight of disability and adding the
Four independent DisMod-MR2.1 inputs were applied to the pro- clinical morbidity associated with a BC diagnosis. Years of life
portion of data obtained from the systematic literature review lost (YLLs) caused by BC have been estimated using global standard
[20]. DisMod-MR2.1 based on Bayesian meta-regression tool, as life expectancy and number of deaths by age [22]. DALYs for BC

Fig. 1. Female breast cancer incidence, death and DALYs (rate per 100 k) in 1990 and 2017 stratified by age group, 15–49years, 50–69years, and 70+years (A) Incidence in
1990 and 2017, (B) death in 1990 and 2017 (C) DALYs in 1990 and 2017.

187
Table 1

S. Mubarik, Y. Yu, F. Wang et al.


Incident cases, Deaths, and DALYs for female breast cancer in 2017 and percentage change of age standardized rates and crude rates by location.

2017 Counts Age-standardised rate % change in Age-standardised Crude rate (per 100 000 % change in crude rate
(per 100 000 population), 2017 rate between 1990 and 2017 population), 2017 between 1990 and 2017
Regions Incidence (95% UI)
Global 1,937,574 (1868019, 2000363) 45.9(44.2,47.4) 17.1(6.2,25.5) 50.9(49.1,52.6) 56.6(41.7,68)
East Asia 380,032 (319781, 410357) 35.9(30.2,38.8) 89.5(30.6,125.9) 52.2(43.9,56.4) 223.3(124.6,286.5)
North Africa and Middle East 90,417 (84474, 99766) 36.9(34.5,41.5) 86.9(28.7,152.7) 31.3(29.3,34.6) 159(77.1,247.8)
South Asia 207,969 (179497, 246149) 27.6(23.8,32.6) 76.7(22.1,138.4) 23.8(20.6,28.2) 141.1(65.4,228)
High-income Asia Pacific 91,510 (85434, 97448) 52.4(49,55.8) 69.9(54,86.4) 96.3(89.9,102.6) 149(125.4,173.5)
Andean Latin America 8216 (7172, 9507) 28.5(24.9,33) 64(28,109.3) 26.8(23.4,31) 142.5(88.3,210.3)
Central Latin America 51,179 (48491, 53899) 39.5(37.4,41.6) 54(42.6,65.9) 39.3(37.2,41.4) 149.6(130.8,168.8)
Southeast Asia 124,436 (114126, 134729) 35.6(32.7,38.5) 44.3(8.2,86.4) 37.6(34.5,40.8) 115.1(59,181.7)
Tropical Latin America 53,787 (51962, 55667) 41.6(40.2,43.1) 40.6(32.7,49.2) 48.1(46.5,49.8) 128.7(115.5,142.8)
Caribbean 14,041 (12497, 15796) 52.6(46.7,59.3) 37(11,65.5) 59.9(53.3,67.4) 97.2(59.8,138.1)
Eastern Europe 96,422 (92737, 100065) 53.2(51.1,55.4) 34.3(23.2,46.9) 85.6(82.3,88.8) 65.1(52.1,79.3)
Central Sub-Saharan Africa 8001(6084, 10539) 24.4(19.3,31.4) 33.4( 29.8,131.8) 13.1(9.9,17.2) 38( 32.7,158.7)
Western Sub-Saharan Africa 45,786 (34747, 60607) 39.4(30.2,51.7) 33.1( 27.6,150.7) 20.7(15.7,27.4) 38.6( 26,164.1)
Central Asia 16,504 (15399, 17691) 35.9(33.6,38.4) 32.6(20,46.5) 35.9(33.5,38.5) 66.5(50.1,84.4)
Central Europe 59,660 (56933, 62745) 59.5(56.8,62.6) 29.8(20.5,40.5) 101.3(96.7,106.5) 76.8(64,91.1)
Southern Sub-Saharan Africa 10,320 (9350, 11228) 30.3(27.4,32.7) 27.7(4.2,51) 26(23.6,28.3) 68.9(39.8,100.2)
Southern Latin America 22,499 (20093, 25353) 52.8(47.1,59.6) 24.3(6.6,45.9) 67(59.8,75.5) 56.5(34.5,83.2)
Oceania 1704 (1265, 2367) 40.7(31.9,53.9) 22( 30,95.4) 27.9(20.7,38.7) 42.2( 25.6,150.5)
Eastern Sub-Saharan Africa 24,819 (21561, 28701) 24.1(21.1,27.9) 13.7( 27.8,66.6) 12.5(10.9,14.5) 20.9( 24.1,81.2)
Western Europe 338,131 (321227, 355134) 86(81.7,90.2) 6.4( 0.8,13.6) 153.4(145.7,161.1) 31(22.3,40)
Australasia 18,659 (16261, 21292) 84.7(73.4,97.2) 5.8( 11.6,25.5) 129.6(113,147.9) 36.8(15.3,61.2)
High-income North America 273,480 (263517, 284405) 92.9(89.2,96.6) 12.6( 17.4, 7.6) 149.2(143.8,155.2) 9.1(3.5,15.4)
Death (95% UI)
Global 600,728 (578725, 629932) 14.1(13.6,14.8) 10.6( 20.8, 1.4) 15.8(15.2,16.6) 22.5(8.3,35.2)
188

South Asia 106,914 (91392, 129439) 15(12.8,18.1) 35.6( 8.4,85.7) 12.3(10.5,14.8) 89(29,162.2)
Central Sub-Saharan Africa 4968 (3861, 6447) 16.5(13.4,20.7) 17.5( 35.2,93.6) 8.1(6.3,10.5) 20.4( 38.8,118.6)
High-income Asia Pacific 18,426 (17651, 19249) 9(8.6,9.4) 17.5(10.6,24.8) 19.4(18.6,20.3) 98.3(87.1,110.3)
Southern Sub-Saharan Africa 5357 (4832, 5767) 16.5(14.9,17.8) 13( 10.9,36) 13.5(12.2,14.5) 52.4(22.3,81.2)
Caribbean 5065 (4442, 5769) 18.8(16.4,21.5) 9.9( 15.8,36.7) 21.6(18.9,24.6) 63.8(25.6,103.7)
Oceania 836 (644, 1140) 23.2(18.9,29.5) 9.3( 33.6,64.9) 13.7(10.5,18.7) 25.8( 31.3,114.2)
Central Asia 6095 (5733, 6471) 13.9(13,14.7) 9.2( 0.2,18.7) 13.3(12.5,14.1) 32(20.6,43.8)
Western Sub-Saharan Africa 25,063 (19362, 32643) 23.9(18.6,30.6) 8.4( 39.6,97.3) 11.3(8.7,14.7) 7.9( 40.8,100.4)
Andean Latin America 3212 (2832, 3687) 11.3(10,13) 7.6( 15.5,36.1) 10.5(9.2,12) 66(30,110.8)
North Africa and Middle East 27,315 (25489, 30742) 11.8(11,13.5) 7.2( 27.1,47.4) 9.5(8.8,10.6) 49(0.3,103.8)
Eastern Europe 32,216 (31323, 33174) 16(15.6,16.5) 3.7( 1.9,9.7) 28.6(27.8,29.4) 32.2(25.2,39.4)
Central Latin America 15,548 (14815, 16320) 12.2(11.6,12.8) 3.4( 3.2,10.3) 11.9(11.4,12.5) 75.6(64.4,87.6)
Southeast Asia 50,199 (46473, 54402) 14.9(13.8,16.2) 1.9( 23.3,31.4) 15.2(14.1,16.5) 57.1(17.2,105.1)
East Asia 90,649 (76202, 97221) 8.6(7.2,9.2) 0( 32.1,18.2) 12.5(10.5,13.4) 81(23.6,114)

Journal of Advanced Research 37 (2022) 185–196


Eastern Sub-Saharan Africa 14,460 (12611, 16779) 15.7(13.7,18) 3.4( 38,39.3) 7.3(6.4,8.5) 0( 37,49.2)
Tropical Latin America 18,886 (18410, 19367) 14.7(14.3,15) 3.7( 7.9,0.8) 16.9(16.5,17.3) 66.5(59.1,74.4)
Central Europe 20,243 (19436, 21083) 17.5(16.8,18.3) 7.8( 13.8, 1.8) 34.4(33,35.8) 38.7(29.6,47.6)
Southern Latin America 8948 (8035, 10059) 19.6(17.6,22.1) 13.7( 24.9, 0.5) 26.6(23.9,29.9) 15(0.4,32.6)
Australasia 4094 (3629, 4576) 16.7(14.8,18.8) 30.8( 40, 20.5) 28.4(25.2,31.8) 4.4( 17.1,9.5)
Western Europe 87,430 (83303, 91614) 18.1(17.2,18.9) 31.4( 35.3, 27.3) 39.7(37.8,41.6) 6.8( 12.2, 1.2)
High-income North America 54,802 (53111, 56588) 17(16.4,17.6) 32.9( 35.8, 29.8) 29.9(29,30.9) 12.6( 16.3, 8.8)
DALYs (95% UI)
Global 17,423,143 (16617465, 18378225) 414.7(395.5,437.6) 9.3( 21.9,2.3) 457.8(436.6,482.9) 18.9(2.3,34.3)
South Asia 3,432,683 (2941453, 4164191) 445.4(381.3,540.1) 35.4( 7.7,88.8) 393.6(337.3,477.5) 79.3(21.4,151.8)
Central Sub-Saharan Africa 165,332 (123344, 218998) 475.7(365.6,620.6) 16.3( 41.9,113.1) 269.8(201.3,357.4) 19.1( 43.6,129.6)
High-income Asia Pacific 470,843 (441005, 501092) 288.9(270.9,306.5) 11.5(0.8,22.1) 495.5(464.1,527.4) 53(38.2,68.2)
Caribbean 143,012 (122890, 166457) 541.8(465.6,632.4) 10.3( 18.8,43) 609.9(524,709.8) 55(13.7,100.8)
Western Sub-Saharan Africa 841,439 (643411, 1109259) 694.2(534.4,906.1) 9.4( 40.3,103.1) 380.1(290.7,501.1) 14.4( 38.2,116.5)
S. Mubarik, Y. Yu, F. Wang et al. Journal of Advanced Research 37 (2022) 185–196

have been computed as the sum of YLDs and YLLs. Specific calcula-
between 1990 and 2017

tion methods are mentioned in the series of articles published by


% change in crude rate

17.7( 24.9, 10.5)


GBD [18,24-26]. As, current study was carried out using Global

17.4( 24.5, 9.5)


25.5( 36.9,132.2)

Burden of Disease Study (GBD) 2017 database and sources are

0.9( 38.3,51.8)

3.7( 10.6,20.7)
11.7( 25.4,3)
38.9(15.1,64.8)

63.7(51.4,76.5)

54.9(46.4,63.8)
19.5(11.7,27.6)
48.9( 1,102.8)

16.6(8.1,25.7)
mentioned in ‘‘Availability of data and materials” statement. The

61(14.5,92.6)
50.8(16.5,94)

30.5(18.3,44)
47.9(8.6,97)
GBD study’s protocol has been approved by the research ethics
board at the University of Washington (UW). The GBD studies must
be conducted in full compliance with UW policies and procedures,
as well as applicable federal, state, and local laws. Therefore, all
ethical standards are justified by properly citing the respective

UR, Uncertainty interval; values are ordered by most to least age-standardised percentage change (excluding global) for each breast cancer indicator (incidence, death and DALYs) separately.
sources (http://ghdx.healthdata.org/gbd-results-tool). Conse-
Crude rate (per 100 000

quently, ethical approval is not required for this study.


866.2(811.2,918.5)
427.6(399.8,459.2)

498.7(483.1,514.6)
768.9(741.2,798.8)

647.6(575.1,733.5)
503.4(366.3,718.5)

308.3(269.1,357.1)

377.1(322.6,407.5)
population), 2017

397.1(363.4,431)

361.3(342.1,381)

255.1(221.8,296)

721.2(632,814.9)

759(718.7,804.2)
509.7(470,551.6)
332(308.1,367)

818(780,859.5)

Statistical analysis

Geographical wise assessment of BC variations was examined


using map construction, stratified by time and age group. We cal-
culated percent change in age-standardised and crude rate of BC
incidence, mortality and DALYs between 1990 and 2017 and pre-
sented the 2017 estimates with 95% uncertainty interval (UI) for
% change in Age-standardised
rate between 1990 and 2017

21 world regions separately. The case-fatality percent (CFP) was


calculated by dividing the age-standardised death rate (ASDR) by
the age-standardised incidence rate (ASIR) and multiplying by
33.3( 39.3, 27.3)
34.4( 40.2, 28.2)
31.5( 42.4, 20)
16.3( 28, 2.5)

100 [27]. Correlation between SDI and CFP was tested using spear-
5.5( 33.4,12.9)
5.8( 40.7,41.3)
14( 20.3, 7)
7.3( 41.4,83.8)
7.2( 28.2,45.8)
5.3( 12.6,24.2)
4.1( 19.4,34.2)

0.2( 25.9,31.7)
2.1( 7.4,3.5)
2.5( 9.3,4.6)

man correlation coefficient (r). The limited cubic splines with three
3.7( 4,11.7)
2.5( 7,12.7)

knots centiles were used to flexibly model the relationship of inci-


dence, mortality, and DALY with SDI values. Further quantile
regression was applied to determine whether the influence of SDI
on BC burden varied in their conditional distributions across quan-
tiles or not [28,29]. BC data of all regions from 1990 to 2017 was
considered for quantile regression analysis.
(per 100 000 population), 2017

In the framework of the age-period-cohort model, the relation-


ship between multiple aspects of BC like incidence, death, case
fatality and DALYs and each of the three primary sources for spatial
Age-standardised rate

and temporal variability: age, period (year), and cohort (year of


452.7(413.1,489.9)

474.9(438.1,513.4)
429.7(416.2,443.4)

257.5(219.3,278.5)

484.2(422.4,548.1)
692.5(530.1,947.9)
379.1(353.1,420.3)

327.7(286.1,380.2)
359.1(340.2,378.5)

482.8(459.5,508.8)

498.5(466.8,530.4)
465.2(405.7,540.2)

492.1(465,521.6)
421.1(394,450.8)

481(462.5,500.3)

birth) were analyzed for each SDI region as well as globally. In


521(462,591.2)

the age-period-cohort analysis, age-specific rates of BC from 20


to 80 years with successive 5-year age interval, and calendar time
including consecutive period from 1990 to 2017, and successive
cohort (period-age) from 1910 to 1997 were considered for statis-
tical analysis. We performed the APC analysis using R package (Epi,
version 2.44) developed by Carstensen et al. 2021 [30]. Rate ratio
was estimated using maximum likelihood (ML) of APC-model Pois-
son with log (Y) based on natural-spline function. Median date of
2,744,523 (2347940, 2966189)

1,390,749 (1316999, 1473569)


1,909,719 (1788436, 2025117)
1,684,759 (1553411,1823089)

birth and median date of diagnosis among cases was chosen for
958,621 (889519, 1059683)

217566.5(193204, 246424)
866,215 (834927, 899837)
470,478 (445493, 496143)

557,150 (539687, 574935)

505,189 (439276, 586266)


157,518 (144145, 170965)

196,394 (183615, 210934)

481,691 (459305, 506173)

reference cohort and period respectively. The goodness of fit was


103,825 (90975, 117310)
94,683 (82634,109651)
30,752 (22374, 43891)

evaluated using the deviance table of estimated models.


2017 Counts

Results

Geographical wise distribution of BC stratified by age group and time

Age-specific geographical distribution of BC incidence, death


and DALYs between 1990 and 2017 were depicted in Fig. 1. Glob-
ally, the incidence rate was increased in all regions between 1990
North Africa and Middle East
Southern Sub-Saharan Africa

High-income North America


Eastern Sub-Saharan Africa

and 2017 among female for the age group of 50–69 years old and
Southern Latin America

above. Particularly, these rates were higher in high SDIs with the
Tropical Latin America
Andean Latin America
Central Latin America

largest increases in High-income North America and Australasia


(Fig. 1A). Besides, death and DALYs rates showed a relatively con-
Western Europe
Table 1 (continued)

Eastern Europe

Central Europe
Southeast Asia

sistent trend. From 1990 to 2017, both rates declined among


Central Asia

Australasia

female aged 50- to 69-year-old and above in high-income North


East Asia
Oceania

America, Australasia, high-income Canada, North America and


South America or Argentina but remained among the highest in
the world (Fig. 1 B & C).
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S. Mubarik, Y. Yu, F. Wang et al. Journal of Advanced Research 37 (2022) 185–196

Change in age-standardized and crude estimates of BC at global and 1990 and 2017 was observed in East Asia. While, deaths and DALYs
regional level were significantly reduced in Australasia, Central Europe, High-
income North America, Southern Latin America, and Western Eur-
Globally, BC among women accounted for 1,937,574 (95% UI: ope between 1990 and 2017. Moreover, the incidence, death and
1868019–2000363) cases in 2017, with an age standardised rate DALYs change in crude rate was raised between 1990 and 2017
(per 100,000) of 45.9 (95% UI: 44.2–47.4), which increased signifi- in all regions except for High-income North America and Western
cantly by 17.1% (95% UI: 6.2–25.5) between 1990 and 2017. It was Europe where death and DALYs were declined in 2017 than 1990
also reported as the cause of death among 600,728 (95% UI: (Table 1).
578725–629932) female in 2017 with an age-standardised death
rate (per 100,000) of 14.1 (95% UI: 13.6–14.8), which decreased Influence of sociodemographic transitions on BC incidence, mortality,
by 10.6% (-20.8 -1.4) between 1990 and 2017. Furthermore, BC case-fatality and DALYs
accounted for 17,423,143 (16617465–18378225) DALYs in 2017,
with an age-standardised rate (per 100,000) of 414.7 (95% UI: When age standardized incidence rate (ASIR), age standardized
395.5–437.6), which was identified as a decrease of 9.3% (-21.9– death rate (ASDR), and DALYs in each world region from 1990 to
2.3) globally between 1990 and 2017. Whereas the death and 2017 were plotted against an index of that region’s sociodemo-
DALYs for crude rate was significantly increased by 22.5% (8.3– graphic status in the same year, different patterns of epidemiolog-
35.2) and 18.9% (2.3–34.3) between 1990 and 2017 (Table 1). ical variations were observed in Fig. 2. In addition to High-income
Out of 21 world regions, only high-income North America had North America, Western Europe and Australia, the incidence of BC
decreased age-standardised incidence rate between 1990 and in different years increase with the increase of SDI, but the mortal-
2017, and highest age-standardised incidence change between ity and DALYs rates showed significant fluctuations. A finite cubic

Fig. 2. Relationship between the age-standardized rates (ASRs, per 100 k) of female breast cancer and SDI over time (1990–2017) by globally and by 21 GBD regions. Each
colored line represents a time trend of the relationship for the specified world regions. Each point represents a specific year for that region. The black line with 95% confidence
band represents the average expected relationship between SDI and ASRs for breast cancer based on values from all countries from 1990 to 2017. The dashed lines represents
the relationship between SDI and ASRs on conditional distributions across quantiles of breast cancer; SDI, social-demographic index; SDI ranges from 0 (less developed) to 1
(most developed).

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S. Mubarik, Y. Yu, F. Wang et al. Journal of Advanced Research 37 (2022) 185–196

Table 2
Quantile regression estimates predicting change in breast cancer due to SDI on conditional distributions across quantiles for the worldwide regions.

Case fatality rate Incidence rate Death rate DALY


Percentiles Coefficient (95 %CI) Coefficient (95 %CI) Coefficient (95 %CI) Coefficient (95 %CI)
5th percentile Intercept 1* (0.95,1.04) 4.79 ( 10.84,1.92) 13.39* (9.27,14.31) 382.26* (278.14,418.47)
SDI 1.13* ( 1.21, 1.04) 50.63* (37.48,64.3) 6.81* ( 8.33, 1.78) 156.14* ( 217.76, 111.82)
25th percentile Intercept 1.02* (1,1.04) 10.25* ( 17.87, 5.09) 17.42* (16.68,17.84) 297.32* (251.93,443.87)
SDI 1.06 ( 1.1, 1.02) 72.08* (61.3,87.38) 9.34* ( 9.97, 8.17) 183.31* ( 109.94,261.9)
50th percentile Intercept 1.01* (1,1.02) 11.98* ( 15.77, 6.27) 13.71* (13.16,14.72) 394.9* (362.68,410.74)
SDI 0.95* ( 0.97, 0.93) 88.46* (77.62,93.75) 3.5* (0.6,4.63) 135.75* (116.62,194.99)
75th percentile Intercept 1.02* (1,1.06) 17.82* ( 20.23, 13.72) 15.82* (14.98,23.19) 486.27* (438.65,666.34)
SDI 0.91* ( 0.97, 0.87) 121.1* (112.69,125.36) 4.86 ( 5.57,6.15) 116.25* ( 12.36,167.92)
99th percentile Intercept 0.97* (0.95,1.51) 16.148 ( 16.3, 15.07) 20.06* (20.02,21.41) 609.2* (606.7,627.68)
SDI 0.64* ( 1.49, 0.59) 161.26* (157.29,162.02) 7.97* (5.72,8.33) 179.55* (154.7,185.17)

DALY, disability adjusted life years; CI, confidence interval; SDI, sociodemographic index; *significant at 1% level of significance.

r = -0.93
r = -0.92
P<0.001
P<0.001

Fig. 3. Time specific correlation between socio-demographic index (SDI) and female breast cancer case-fatality percent (CFP) in 1990 and 2017 worldwide. Case-fatality
percent was calculated by dividing age-standardised death rate by age-standardised incidence rate and multiplied by 100, r represent the correlation coefficient between SDI
and CFP among world regions, LSE, Least Square Error fit; LAE, Least Absolute Error fit; SDI(%) ranges from 0 (less developed) to 100 (most developed).

spline with three nodes was used to flexibly simulate the relation- r1990 = 0.92, P < 0.001) in both 2017 and 1990 around the globe
ship between age-standardized rates (ASR) with SDI. The estimated and the highest case fatality percentage was observed in Central
relationship between SDI and ASR of BC incidence, mortality, and Sub-Saharan Africa (Fig. 3).
DALYs, shown as the black line in Fig. 2, was a gradual increase
for ASIR as SDI increases, with more rapid growth at the highest Age-period-cohort effects on BC incidence, death, DALYs and case-
levels of SDI. The reverse trend in ASDR and DALYs was found, fatality
decreasing first and then increasing, but this trend was not obvi-
ous. We observed negative association between SDI and death in We estimated the age period cohort trends in BC for each SDI
25th and below percentiles of death rate for the worldwide region and globally, which captures age, period and cohort effects.
regions. While for countries with DALYs in 25th and above per- Each of these effects, holding all other variables constant at their
centiles have increase in DALYs with the increase of SDI but for sample mean values, as shown in Fig. 4. For each SDI region and
countries with DALYs in 5th percentile, DALYs has decrease with the global age-related impacts, it can be easily seen that BC burden
increase of SDI. The change in BC parameter due to SDI in specific ((A) incidence, (B) death and (C) DALYs) almost in all regions con-
percentiles has depicted in Table 2. The incidence, death and DALY tinue to grow with age, and the risk of BC burden tend to increase
had increase by 88.46 (95 %CI: 77.62, 93.75), 3.5 (0.6, 4.63) and most remarkably in low SDI regions. The analysis exposed increase
135.75 (95 %CI: 116.62, 194.99) respectively due to unit increase incidence risk trend with increase birth cohorts from the median
in SDI on 50th percentile of parameters. date of birth among cases, in each SDI regions. The risk value for
Additionally, there was observed a strong negative correlation death and DALYs was decreasing in high-SDI to middle-SDI
between SDI and case fatality percent (r2017 = 0.93, P < 0.001; regions, and it was increasing in low-middle to low-SDI regions
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S. Mubarik, Y. Yu, F. Wang et al. Journal of Advanced Research 37 (2022) 185–196

Fig. 4. Age period cohort related female breast cancer trends in (A) incidence rate (B) death rate and (C) DALYs from 1990 to 2017 with ages 20 to 80. Rate ratio was estimated
using ML of APC-model Poisson with log(Y) based on natural-spline function, for each SDI region separately. DALYs, disability adjusted life years; ML, maximum likelihood;
APC, age-period-cohort; Reference cohort for age-effects was chosen as the median date of birth among cases; Median date of diagnosis among cases was selected as
reference period.

Fig. 5. Age period cohort trends in case-fatality rate of female breast cancer from 1990 to 2017 with ages 20 to 80. Rate ratio was estimated using ML of APC-model Poisson
with log(Y) based on natural-spline function, for each SDI region separately. ML, maximum likelihood; APC, age-period-cohort; Reference cohort for age-effects was chosen as
the median date of birth among cases; Median date of diagnosis among cases was selected as reference period.

from the reference cohort (median date of birth among cases) to Discussion
onward (Fig. 4).
We also conducted APC analysis on case-fatality rates (CFR) in GBD-based studies reveal the most up-to-date patterns and
different SDI regions. As shown in Fig. 5, overall, risk of case- trends of the incidence, mortality, DALYs and related socioeco-
fatality rate tends to decrease most noticeably in high middle SDI nomic risk factors associated with the onset and development of
countries, and the reduction of the risk of case-fatality rate in the BC worldwide. Breast carcinogenesis involves a complex interplay
recent cohort was the lowest in the low SDI countries. The effect of various genetic, environmental, socioeconomic and lifestyle risk
separation was more obvious between different SDI regions on factors. Since 1990, ssocioeconomic development linked disparities
age greater than 50 years and for cohort 1960 to forward. The per- in the global BC incidence have continued to decrease. However, as
iod effect remained consistent during the entire duration in all SDI per SDI, highly developed regions showed greater BC incidence
regions and globally (Fig. 5). burden by 2017. In the recent years, consistently the reverse trends

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S. Mubarik, Y. Yu, F. Wang et al. Journal of Advanced Research 37 (2022) 185–196

in mortality rates among high and low SDI countries showed that might be attributed to the lesser use of postmenopausal hormonal
the mortality intensity indicators become negative amongst treatment after the availability of Women’s Health Initiative Trial
women aged 15–49 and 50–69 years [31]. These circumstances as this hormonal usage is linked with elevated BC risk [42].
are possibly due to shift in the burden of BC mortality from high- Additionally, this continuous decline or stabilization has been
income to middle- and low-income countries. In the current study characterized to advancement in mammographic screening, BC
we have examined the age period and cohort trends in multiple diagnosis at earlier stages and better treatment facilities in terms
aspects of BC including incidence, death, case fatality and DALYs of chemotherapeutics, radiation therapy and targeted approaches
among females and assess the association of these aspects with [6]. Moreover, we have observed that case fatality burden keeps
sociodemographic transition across 21 world regions based on on declining from 1990 to 2017 in most of the high and high mid-
GBD data from 1990 to 2017. dle SDI regions like North America, Asia pacific, Austrasia and Wes-
We have observed an increased incidence of BC with age stan- tern Europe illustrating the fact that high income regions have
dardised rate (per 100 k) of 45.9 in 2017 all over the world. better treatment facilities. Whereas Central Sub-Saharan Africa,
Whereas a decrease is observed in the age standardised death rate Eastern Sub-Saharan Africa, Western Sub-Saharan Africa, Oceania,
(per 100 k) of BC cases between 1990 and 2017. Moreover, we have Southern Sub-Saharan Africa and South Asia have high case fatality
found that the death and DALYs for crude rate was significantly rate being less developed regions with limited disease diagnosis
increased by 22.5% and 18.9% respectively between 1990 and and treatment resources.
2017. Out of twenty-one regions, only high-income North America APC analysis recognizes patterns of cancer incidence/mortality
had reduced age-standardised incidence rate (per 100 k), while rates from population-based count and data. Group of people born
deaths and DALYs were significantly decreased in Australasia, Cen- in the same generation is called as age cohort. An aging effect is
tral Europe, High-income North America, Southern Latin America, described as a shift in variable values that happens among all the
and Western Europe in the said time duration. cohorts separately of time period, as each cohort grows older. A
Besides, an increase in the incidence, death and DALYs was cohort effect is an alteration which exemplifies different popula-
observed among crude rate between 1990 and 2017 in all tions born at a specific point in time, but it is independent of aging
twenty-one regions except for High-income North America and procedure. Whereas a period effect is a change which occurs at a
Western Europe where a declining trend was found in death and specific time, influencing equally cohorts and all age groups.
DALYs in 2017 than 1990. Global cancer burden 2017 attributed Results for each SDI region and the global impact of age showed
the variations in BC incident rates to population growth and aging that BC burden (incidence, mortality and DALYs) increases with
process [32]. Various other studies have also supported the find- age in all regions and this trend was more pronounced in the high
ings that being a complex chronic systemic disease, BC likely to SDI regions. The period trend keeps on fluctuating in all popula-
have significant association with age, as disease incidence tions, with higher instabilities in low SDI areas, but the overall
increases with increased age [33-37]. Decreased deaths and DALYs results are not much variable. Else, inconsistent trend among the
among developed countries were attributed to the adoption of incidence, death and DALYs rates of BC was displayed by the cohort
widespread mammographic screening of the disease [15,33]. When effects. Globally, declining death trends of BC were depicted by
we stratified the geographical distribution of BC by time and age cohort. The effect in high SDI quantile was similar to the global
group it was found that it is more prevalent among females above trend, but the downward trend was more obvious, followed by
the age of 50 years all around the world being hormonally sensitive high-middle and middle SDI regions, which showed a downward
cancer [38]. Additionally, disease was more common in high SDI risk trend as a whole, whereas in low-middle and low SDI regions,
countries specifically in North America and Australasia with overall, this risk for BC increased slightly. All these findings again
declining death and DALYs trends possibly due to advancement highlight the potential development of breast diagnosis, prognosis
in BC treatment methodologies. and treatment and suggesting that better diagnostic tools along
Universally, with higher than 2 million new BC diagnoses every with easy access of treatment modalities all over the world can
year, attempts to improve early detection and treatment resonate help in decreasing the global BC burden [6,43,44].
deeply with cases, clinicians and surgeons alike. Though the five To enhance our findings, we have conducted APC analysis on
year survival rate of female BC cases has increased, notably in high case-fatality rates (CFR) separately for different SDI areas. Consis-
SDI regions, over the last 3 decades, the disease burden of BC tently, the age, period, and cohort effects of CFR were greater in
among women still remained elevated in most of the regions [3]. low SDI as compared to high SDI, but the effect separation was
This is mainly attributed to the constantly increased BC incidence found to be more evident amongst different SDI regions with age
among women. In the current study, we have found that ASIR of greater than 50 years and for cohort 1960 to onward. Furthermore,
BC among women continued to increase in most of the high SDI the overall case fatality risk trend was escalating with increased
countries along with Asian and African regions with previously les- age and risk value was obviously greater in low SDI countries with
ser BC rates [39]. This increasing ASIR trends are alarming and reverse findings in high SDI regions. Our findings have shown that
thought to signify the increased prevalence of known BC related the overall cohort pattern gradually decreases from early to late
risk factors like adopting western lifestyle, diet changes, reduced cohort. Whereas the period effect continued to be consistent glob-
physical activity and various reproductive patterns. Another possi- ally during the entire duration.
ble reason behind this increasing trend might be the availability of We have suggested that country specific information on cancer
routinely and extensively performed mammography, awareness burden is required for the policy makers to evaluate the influence
campaigns and access to health care systems. Mammographic of cancer registries, control programs, standard of national pro-
screening unavoidably necessitates increased BC incidence due to gress, limited access to health care systems and provide a better
early detection of BC among women that would otherwise have plan to combat with the disease. Bearing in mind the fact that pre-
been diagnosed in the later stages of life or remain unidentified vailing data in many countries is missing or of low quality, and
throughout the life [40]. One of the studies has shown that BC diag- most of the data was based on individual hospital registries and
nosis at early stages has been doubled in the age group of 50– records as they lack national level registries, results from the
69 years due to the introduction of mammographic screening dur- GBD study can be used by stakeholders to explore the disease pat-
ing 2003–2014 [41]. We have also found that ASIRs decline or tern of different countries in their corresponding locations.
remain stable in some of the countries and this declining trend GBD studies comes up with comprehensive quality global dis-
was also obvious for ASDR and DALYs. These declining trends ease burden estimates yet they have some limitations depending
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S. Mubarik, Y. Yu, F. Wang et al. Journal of Advanced Research 37 (2022) 185–196

upon the data collection procedures, treatment methodologies and Declaration of Competing Interest
individual biasness. Differences or ambiguities in data collection
procedures its coding, handling and quality of the sources from The authors declare that they have no known competing financial
where data has been collected (hospital records / national reg- interests or personal relationships that could have appeared to influ-
istries) remains unavoidable in any analysis pattern. In addition, ence the work reported in this paper.
variations in the incidence and mortality rates may partially repre-
sents the detection biasness linked with the screening and diag- Acknowledgments
nostic protocol’s modifications rather than factual changes in age
specific rates. Besides this another inevitable limitation is the This project was supported by the National Key R&D Program of
unavailability of proper data from many of the undeveloped or China and the National Natural Science Foundation of China, we
under developing countries causing misleading findings, although would like to thank the funding foundations for their support.
GBD keeps on filling the gaps in the data throughout the year to
provide accurate disease patterns.
Availability of data and materials

Conclusion The dataset analyzed during the current study are available in
the Institute for Health Metrics and Evaluation (IHME): http://
BC remains a major health issue among women around the ghdx.healthdata.org/gbd-results-tool.
globe and responsible for highest number of cancer-related mor-
bidity and mortality. Globally, BC burden continues to increase
from 1990 to 2017 and linked with increasing age as well, whereas Appendix A. Supplementary material
the age standardized death rates and DALYs rates has been declin-
ing. In the recent years, disease burden has been reduced in most of Supplementary data to this article can be found online at
the high SDI regions, but incremental disease burden has been https://doi.org/10.1016/j.jare.2021.07.012.
observed in middle and low SDI regions and there may be a contin-
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regional, and national comparative risk assessment of 84 behavioural, Ms. Sumaira Mubarik is a final year PhD researcher at
environmental and occupational, and metabolic risks or clusters of risks, Wuhan University, China. She has published more than
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The Lancet. 2017;390(10100):1345–422. international journals, including, The Lancet, The Lan-
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regional, and national incidence, prevalence, and years lived with disability for Cardiology, International journal of epidemiology,
328 diseases and injuries for 195 countries, 1990–2016: a systematic analysis Frontiers in Medicine, Scientific Reports, Cancer Com-
for the Global Burden of Disease Study 2016. The Lancet. 2017;390 munications, Clinical Epidemiology etc. She’s also col-
(10100):1211–59. laborator in Global burden of disease study projects,
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https://doi.org/10.1186/s13045-019-0799-1. graduated from Wuhan University of technology in June
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(6):703–30. epidemiology and disease burden research, software
[25] Murray CJ. Quantifying the burden of disease: the technical basis for disability- development, data mining and processing, proficient in
adjusted life years. Bull World Health Organ 1994;72(3):429. PHP, R, Python, C#, VB, and published more than 30
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associated with national human development index and health system Dr. Fang Wang has received her PhD degree in Statistics
attainment. PloS one 2016; 11(7). from Wuhan University, Wuhan, China in the year 2021.
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breast cancer incidence and mortality according to sociodemographic indices: 30 research papers in well-reputed journals, including
an observational study based on the global burden of diseases. BMJ open. International journal of epidemiology, Journal of the
2019;9(10):e028461. doi: https://doi.org/10.1136/bmjopen-2018-028461.
American College of Cardiology, The Lancet, Cancer
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Communications, and Scientific Reports etc.
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cancer susceptibility gene: evidence from genetic profiling, statistical Dr. Saima Shakil Malik is a biologist and a postdoctoral
inferences and protein structural analysis. Breast Cancer. 2020;27(6):1168–76. researcher at University of Alabama at Birmingham. She
[35] Ma X, Liu C, Xu X, Liu L, Gao C, Zhuang J, et al. Biomarker expression analysis in received her PhD degree in Cancer genetics from Fati-
different age groups revealed age was a risk factor for breast cancer. J Cell
mah Jinnah Women University, Pakistan, in 2020. She
Physiol 2020;235(5):4268–78.
has developed research in cancer genetics, epidemiol-
[36] Mubarik S, Wang F, Fawad M, Wang Y, Ahmad I, Yu C. trends and projections in
ogy, pathology, DNA repair mechanisms and post
Breast cancer Mortality among four Asian countries (1990–2017): Evidence
from five Stochastic Mortality Models. Sci Rep 2020;10(1):1–12. translational modifications. She is an editor of a book,
[37] Mubarik S, Malik SS, Wang Z, Li C, Fawad M, Yu C. Recent insights into breast author of several book chapters and various scientific
cancer incidence trends among four Asian countries using age-period-cohort publications.
model. Cancer Manage Res 2019;11:8145.
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breast cancer incidence at the global, regional, and national levels, 1990–2017.
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International variation in female breast cancer incidence and mortality rates.
Cancer Epidemiol Biomarkers Prev 2015;24(10):1495–506.
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mammography screening. J Public Health Policy 2015;36(3):259–69.
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incidence and mortality before and after implementation of the German
mammography screening program. Int J Cancer 2020;147(3):709–18.

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S. Mubarik, Y. Yu, F. Wang et al. Journal of Advanced Research 37 (2022) 185–196

Ms. Xiaoxue Liu is final year PhD Scholar at Wuhan Ms. Fang Shi is a final year PhD Scholar at Wuhan
University, Wuhan, China. She has many important University, Wuhan, China. She has published more than
contributions towards cancer science and epidemiology 10 research papers in well-reputed journals, including,
published by various well-known publishers. Preventive Veterinary Medicine, Cancer Communica-
tions, International journal of epidemiology, Frontiers in
Medicine, and Cancer Management and Research etc.

Dr. Muhammad Fawad has received his PhD degree in Prof. Dr. Chuanhua Yu is currently working at
Mathematical Statistics from Central China Normal Department of Epidemiology and Biostatistics, School of
University, Wuhan, China in 2019. Currently, he is Health Sciences, Wuhan University, Wuhan, China. He
working as a Postdoctoral researcher at Zhengzhou Key completed his PhD in Biostatistics at The Fourth Military
Laboratory of Big Data Analysis and Application, Henan Medical University, Xi’an, China. His main research
Academy of Big Data, and School of Mathematics and interests include Method and application for Global
Statistics, Zhengzhou University, Zhengzhou, China. His Burden of Disease and Statistical methods in decision
research interests include Applied Probability, Robust making for medical research. He has developed various
Estimation Methods, Mathematical Statistics and research projects, have many national and international
developed various research articles within these grants, and produced several postgraduate and PhD
research areas. dissertations. He has published dozens of research
articles in peer-reviewed international journals and
authored or co-authored various books.

196

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