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Research paper 1
Mortality trends and prediction of HPV-related cancers
in Brazil
Dyego L.B. de Souzaa, Maria Paula Curadob,e, Marı́a Milagros Bernalc,
Javier Jerez-Roigd and Paolo Boffettab
Estimation of the size of a cancer group, either through
number of cases or extrapolation of past observed trends,
is indispensable to the planning of effective assistance
measures. The aim of this study was to analyze the
mortality trends of human papillomavirus-related cancers
in Brazil by sex, in the period 1996–2010, and make
predictions until the year 2025. All deaths registered as
being a result of cervical cancer (ICD-10 code: C53), as well
as those caused by vulvar and vaginal (C51 and C52), anal
(C21), penile (C60), and oropharyngeal (C02, C09, C10)
cancers, were registered. Adjusted rate calculations for
each year were used to study the trends through the
regression program ‘Joinpoint’. Predictions were made
using the Nordpred program, utilizing the age–period–cohort
model. When analyzing separately by location, it was
observed that penile and anal cancers in men presented an
increasing trend for the entire period with a statistically
significant annual percentage change of 4% for anal cancer
and 1.4% for penile cancer. Predictions indicate a reduction
in the risk of death due to oropharyngeal cancer in men
and cervical, vulvar, and vaginal cancers in women. It was
observed that the increase in the number of deaths occurs
mainly because of population changes (size and age
structure). In terms of risk, an increase is predicted for anal
and penile cancers in men and consequently an increase
in mortality rates is observed for these types of cancers,
unlike what is expected for human papillomavirus-related
cancers in women. European Journal of Cancer Prevention
c 2013 Wolters Kluwer Health | Lippincott
00:000–000 Williams & Wilkins.
Introduction
also be related to HPV, such as oral cavity, laryngeal, and
nasopharyngeal cancers, although causal evidence is not
as strong as that for the oropharyngeal cancer (Gillison
et al., 2000; Chung and Gillison, 2009).
Infectious agents play a fundamental role in the
development of some types of cancer, and among these
agents, human papillomavirus (HPV) has received
particular attention, establishing itself as an etiological
agent in skin or mucous keratinocytes. There are
innumerous genotypes of this virus, serotypes 16 and 18
being the most frequently associated with genital and oral
carcinogenesis. The virus is transmitted mainly through
sexual contact and, besides cancer, can cause benign
lesions such as genital warts (Jung et al., 2004).
Estimates for the year 2008 show that 660 000 cases of
cancer were related to HPV, and the highest prevalence is
observed in developing nations. For developed countries,
it is estimated that HPV-related cancers represented
B29% of all malignant tumors associated with infections
(De Martel et al., 2012).
A review of scientific evidence carried out by experts at
the International Agency for Research on Cancer shows
that the types of cancers related to HPV are cervical,
penile, vulvar, vaginal, and oropharyngeal (including
tonsils and the base of the tongue) cancers (IARC
Working Group on the Evaluation of Carcinogenic Risks
to Humans, 2011). Other head and neck cancers could
c 2013 Wolters Kluwer Health | Lippincott Williams & Wilkins
0959-8278 European Journal of Cancer Prevention 2013, 00:000–000
Keywords: Brazil, cancer, human papillomavirus, mortality, prediction, trends
a
Department of Public Health, Federal University of Rio Grande do Norte, Natal,
Goiania Population-Based Cancer Registry, Goias, Brazil, cDepartment
of Microbiology, Preventive Medicine and Public Health, University of Zaragoza,
d
Can Misses Hospital, Ibiza, Spain and eInternational Prevention Research
Institute – IPRI, Lyon, France
b
Correspondence to Dyego L. B. de Souza, PhD, Department of Public Health,
Federal University of Rio Grande do Norte, Gel. Cordeiro de Farias Avenue
s/n, 59010-000, Petropolis, Natal - RN, Brazil
Tel: + 55 84 33429750; fax: + 55 84 32215365; e-mail: [email protected]
Received 17 August 2012 Accepted 16 September 2012
The epidemiological situation of HPV-related cancer in
Brazil is still not very well explored. The prevalence of
HPV in the country is B25% in women younger than 35
years of age, and it decreases with age (Nonnenmacher
et al., 2002; Rama et al., 2008). In men, the prevalence is
superior to that in women, B72% (HPV Study Group in
Men from Brazil, USA and Mexico, 2008).
Estimation of the size of a cancer group, either by the
number of cases or extrapolation of past observed trends,
is indispensable to the planning of effective assistance
measures. The objective of this study was to analyze the
mortality trends of HPV-related cancers in Brazil by sex,
for the period 1996–2010, and make predictions until the
year 2025.
Methodology
All deaths registered as being a result of cervical cancer
(ICD-10 code: C53), as well as those due to vulvar and
vaginal cancers (C51 and C52), anal (C21), penile (C60),
and oropharyngeal (C02, C09, C10) cancers, were
DOI: 10.1097/CEJ.0b013e32835b6a43
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
2 European Journal of Cancer Prevention 2013, Vol 00 No 00
included in the
Brazilian Health
tion data from
certificates was
codes.
related to the last observed period (2006–2010) were
calculated by topography and sex. The proportion of this
change occurring in terms of risk or change in population
(size and population structure) was also calculated.
These two components can be different from zero and
present a positive or negative direction. The calculation
can be expressed as follows (Møller et al., 2002, 2003):
analysis. Data were obtained from the
Ministry web page, along with popula1996 to 2010. The quality of death
good, with less than 20% ill-defined
Analyses of mortality and predictions were carried out by
calculating crude and adjusted rates for each sex,
expressed per 100 000 persons/year. The adjusted rates
were calculated by the direct method using the world
standard population as a reference. Adjusted rates for
each year were calculated to study the trends through the
regression program ‘Joinpoint’ (National Cancer Institute, Bethesda, Maryland, USA). The objective was to
determine whether the estimated trends are statistically
significant or not. Joinpoint analysis identifies the
moment at which changes in trends occur and calculates
the annual percentage change (APC) in each segment.
The analysis starts with a minimum number of joinpoints
and estimates whether one or more are significant with
regard to the model (Kim et al., 2000). Birth cohort
analysis was carried out graphically on the basis of sex and
by dividing data into 5-year periods.
Dtot ¼Drisk þDpop ¼ðNfff Noff ÞþðNoff Nooo Þ;
where Dtot is the total change, Drisk is the change as a
function of risk, Dpop is the change as a function of
population, Nooo is the number of observed cases, Nfff is
the number of predicted cases, and Noff is the number of
expected cases when the mortality rates increase during
the observed period.
The populations used in the projections were obtained
from the website of the Brazilian Statistics and
Geography Institute (IBGE, 2012).
Results
Between 1996 and 2010, 99 870 deaths because of HPVrelated cancers were registered. Joinpoint analysis yielded
similar results for both sexes when all combined locations
were analyzed. Initially, an increasing trend was observed
in mortality rates, thereafter, a decreasing one, with a
change point in 2005 (Fig. 1). On analyzing separately by
location, it was observed that penile and anal cancers in
men presented an increasing trend for the entire period,
with a statistically significant annual percentage change
of 4% for anal cancer and 1.4% for penile cancer. The
oropharyngeal region in women was the only location for
which a change point was not identified, and the
observed rates were stable (Table 1).
Predictions were made on the basis of sex for the periods
2011–2015, 2016–2020, and 2021–2025 utilizing the age–
period–cohort model of the Nordpred program (Cancer
Registry of Norway, Oslo, Norway), written in the
statistical program R. Data were pooled into 5-year
blocks and the limit age group considered for analysis was
the one with more than 10 cases in the combined periods.
Predictions were made by cancer site and the pooled
results will be referred to as the total, presented by age
ranges (0–54, 55–74, and Z 75 years of age). Changes in
the annual number of cases of the last predicted period
Fig. 1
7
Males
Females
Rate per 100 000
6
APC1 = 0.77
5
APC2 = −2.90∗
4
3
2
APC1 = 1.94∗
APC2 = −0.92
1
09
08
10
20
20
07
06
20
20
20
04
05
20
03
02
01
20
20
20
20
00
98
99
20
19
97
19
19
19
96
0
Trends in mortality-adjusted rates for human papillomavirus-related cancers in Brazil. Rates in 100 000 persons/year and annual percent change
(APC). *Statistically significant.
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Mortality trends and prediction of HPV-related cancers de Souza et al. 3
Table 1
Number of deaths, annual percentage changes, 95% confidence intervals, and joinpoint year in men and women
Men
Anal (C21)
Penile (C60)
Oropharyngeal including tonsils and the base of the tongue (C01, C09–C10)
Total
Women
Anal (C21)
Cervical (C53)
Vulvar (C51) and vaginal (C52)
Oropharyngeal including tonsils and the base of the tongue (C01, C09–C10)
Total
Number of deaths
APC1
951
3722
21 116
25 789
4.0a
1.4a
1.9a
1.9a
1875
63 763
4864
3579
74 081
5.3a
0.6
0.5
0.9
0.8
95% CI
Joinpoint
APC2
95% CI
2.3/5.7
0.6/2.2
0.8/2.9
0.8/3.1
–
–
2005
2005
–
–
– 1.4
– 0.9
–
–
– 3.9/1.3
– 3.6/1.8
2.2/8.4
– 0.5/1.8
– 0.7/1.8
– 0.3/2.1
– 0.3/1.9
2005
2005
2006
–
2005
– 3.8
– 3.1a
– 2.4
–
– 2.9a
– 10.5/3.4
– 5.8/ – 0.3
– 7.3/2.7
–
– 5.4/ – 0.3
APC, annual percentage changes; 95% CI, 95% confidence intervals.
a
Statistically significant.
In the birth cohort analysis, it was verified that the trend
change point was not maintained in the younger cohorts,
since 1958, of men and women, in which a reduction or
stability in mortality rates is already observed (Fig. 2).
Table 2 presents the number of cases, adjusted rates for
the observed period, and predictions for the periods
2011–2015, 2016–2020, and 2021–2025 by sex. For men,
10 460 deaths were registered in the last observed period
(2006–2010), and according to the predictions, there will
be an increase in the number of deaths to 14 391 in
2021–2025. For women, the number of deaths for the last
observed period was 28 495, and an increase in predictions to 35 642 in 2012–2015 was also observed. In terms
of mortality rates, a decrease was observed for both sexes
starting from the last observed period and maintaining
itself throughout predictions.
An aging process of the Brazilian population is expected,
which can be verified by comparing the population
distribution by age group in the last observed period
with the population prediction for 2012–2015 (Fig. 3),
according to IBGE data.
Table 3 shows a comparison between the number of
deaths registered in the last observed period and
predictions based on the number of deaths in the last
predicted period. The calculation performed for the
annual change relative to risk or population changes (size
and structure) showed a reduction in the risk of death for
oropharyngeal cancer in men and cervical, vulvar, vaginal,
and anal cancers in women. For these types of cancers,
there will be an increase in the number of deaths,
although because of population changes. An increase in
the risk of death was observed for penile and anal cancers
in men and oropharyngeal cancer in women.
Discussion
It is known nowadays that HPV infection plays an
important role in the development of cervical cancer, as
well as anal, penile, vaginal, and oropharyngeal (including
tonsils and the base of the tongue) cancers. However, the
prevalence of HPV varies in accordance with the location
of the tumor. For cervical cancer, for example, HPV is
strongly associated and represents a necessary cause for
the development of this type of cancer (Bosch et al.,
1995). Anal carcinoma is also strongly associated with
HPV, with the prevalence of the virus in B88% of cases.
For the oropharynx and other locations, the prevalence of
HPV is more variable and depends on the population
studied. It is estimated that the prevalence of HPV is
56% in oropharyngeal cancers in North America, 52% in
Japan, and in developing countries such as Brazil, this
percentage would be B13% (De Martel et al., 2012). For
penile, vulvar, and vaginal cancers, the approximate
prevalence of HPV in tumors is 50, 43, and 70%,
respectively (Backes et al., 2009; De Vuyst et al., 2009).
Among the cancers studied herein, oropharyngeal cancer
must be treated separately because of its differentiated
epidemiological profile. This type of cancer presents as
the main risk factors consumption of tobacco and alcohol,
and just recently, the association of HPV with the
development of these tumors was shown. Research from
different countries shows an increase in oropharyngeal
cancer trends, including the base of the tongue and
tonsils (Chaturvedi et al., 2008; Auluck et al., 2010; De
Souza et al., 2012), and the number of oropharyngeal
cancer cases related to HPV is probably higher in
countries in which the consumption of tobacco and
alcohol is lower (De Camargo Cancela et al., 2012).
The recent decrease in the mortality due to oropharyngeal
cancer verified in men may be occurring because of a
reduction in the consumption of tobacco in Brazil. The
prevalence of tobacco consumption among Brazilian men
has reduced since the late 1980s, and since 2003, tobacco
consumption has become more pronounced in women
(Wünsch Filho et al., 2010). In contrast, data from the Food
and Agriculture Organization of the United Nations
showed that alcohol consumption in Brazil has followed
an increasing trend (FAO: Statistics, 2012). Therefore, for
oropharyngeal cancer, it is necessary to also consider these
changes in risk factor trends when analyzing the results of
this study and establishing hypotheses.
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
4 European Journal of Cancer Prevention 2013, Vol 00 No 00
Fig. 2
Males
90
80
Rate per 100 000
70
60
50
40
30
20
10
73
68
19
63
19
58
19
19
53
19
19
48
43
19
38
33
19
23
28
19
19
19
18
19
19
13
0
Females
250
Rate per 100 000
200
150
100
50
73
19
68
19
19
63
58
19
53
19
48
19
43
19
38
19
33
19
28
19
23
19
18
19
19
13
0
Year of birth
80–84
75–79
70–74
65–69
60–64
55–59
50–54
45–49
40–44
35–39
Trends by birth cohort in men and women.
When analyzing predictions, it is necessary to differentiate between two situations that may lead to increases or
decreases in the number of deaths or mortality rates:
changes in exposition of risk factors and/or population
exposed to risk. Changes in the population exposed to
risks can occur because of an increase in the population as
well as the age structure of the population (Bray and
Møller, 2006; De Souza et al., 2011). In Brazil, governmental predictions indicate an increase in the total
population and changes in age groups. The aging process
experienced by the Brazilian population, resulting from
a reduction in fertility and an increase in life expectancy,
and common to other Latin American countries, was
accelerated and will continue in the future. Until the
1960s, the demographical characteristics were those of a
young country, with high fertility rates, and from this
point, the demographical transition and population aging
started. The proportion of elderly individuals increased
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Mortality trends and prediction of HPV-related cancers de Souza et al. 5
Table 2
Observed and predicted average annual number of deaths by age, and world age-standardized rates in Brazil
Observed
1996–2000
Men
Penile (C60)
Age
0–54
371
55–74
376
Z 75
227
Total
974
ASW
0.32
Anal (C21)
Age
0–54
61
55–74
107
Z 75
38
Total
206
ASW
0.07
Oropharyngeal (C01, C09–C10)
Age
0–54
2202
55–74
2897
Z 75
555
Total
5654
ASW
1.95
Total
Age
0–54
2634
55–74
3380
Z 75
820
Total
6834
ASW
2.34
Women
Cervical (C53)
Age
0–54
9171
55–74
6847
Z 75
2140
Total
18 158
ASW
5.23
Vulvar and vaginal (C51, C52)
Age
0–54
235
55–74
555
Z 75
509
Total
1299
ASW
0.37
Anal (C21)
Age
0–54
97
55–74
222
Z 75
89
Total
408
ASW
0.12
Oropharyngeal (C01, C09–C10)
Age
0–54
235
55–74
460
Z 75
244
Total
939
ASW
0.28
Total
Age
0–54
9738
55–74
8084
Z 75
2982
Total
20 804
ASW
6.00
Prediction
2001–2005
2006–2010
2011–2015
2016–2020
2021–2025
455
454
271
1180
0.33
531
646
391
1568
0.36
580
798
447
1824
0.37
639
996
558
2193
0.38
658
1206
718
2582
0.39
111
142
69
322
0.09
145
192
86
423
0.10
155
247
89
491
0.10
169
320
95
584
0.10
186
383
114
684
0.11
2670
3586
791
7047
2.09
3013
4404
998
8415
2.01
2960
5046
1102
9108
1.91
2865
5896
1266
10 026
1.81
2915
6559
1519
10 992
1.72
3236
4182
1131
8549
2.51
3689
5242
1475
10 406
2.47
3748
6104
1640
11 491
2.40
3784
7212
1910
12 907
2.32
3901
8173
2317
14 391
2.23
10 462
8183
2752
21 397
5.24
11 217
9325
3666
24 208
4.75
11 674
9840
3931
25 445
4.35
12 173
10 657
4600
27430
4.09
13 096
11 490
5339
29 925
3.95
272
644
681
1597
0.37
310
741
917
1968
0.35
331
807
1027
2164
0.34
328
947
1220
2495
0.32
326
1136
1396
2858
0.31
168
295
196
659
0.16
178
379
251
808
0.16
192
393
291
876
0.14
165
472
333
970
0.13
195
509
362
1067
0.13
325
519
285
1129
0.28
357
657
496
1510
0.29
425
770
569
1764
0.29
420
954
715
2089
0.29
450
1117
858
2425
0.29
11 227
9641
3914
24 782
6.05
12 062
11 102
5331
28 495
5.54
12 510
11 798
5784
30 093
5.10
12 846
12 943
6832
32 622
4.78
13 570
14 114
7958
35 642
4.58
ASW, age-standardized rates.
from 9.1 to 11.3% between 1999 and 2009, constituting,
at present, a contingence of over 22 million people.
Between 1997 and 2007, the number of individuals older
than 80 years of age increased by 47.8%, and in the age
group of 60–69 years, the increase was by 21.6% (IBGE,
2012).
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
6 European Journal of Cancer Prevention 2013, Vol 00 No 00
Fig. 3
Males
10 000 000
9 000 000
8 000 000
7 000 000
6 000 000
5 000 000
4 000 000
3 000 000
2 000 000
1 000 000
85
+
0–
4
5–
9
10
–1
4
15
–1
20 9
–2
4
25
–2
9
30
–3
4
35
–3
9
40
–4
45 4
–4
9
50
–5
4
55
–5
60 9
–6
4
65
–6
9
70
–7
75 4
–7
9
80
–8
4
0
Females
10 000 000
9 000 000
8 000 000
7 000 000
6 000 000
5 000 000
4 000 000
3 000 000
2 000 000
1 000 000
2006–2010
85
+
0–
4
5–
10 9
–1
4
15
–1
20 9
–2
4
25
–2
30 9
–3
4
35
–3
40 9
–4
4
45
–4
9
50
–5
4
55
–5
9
60
–6
4
65
–6
70 9
–7
4
75
–7
9
80
–8
4
0
2021–2025
Changes in the distribution of the Brazilian population between men and women.
The results indicate that the increase in the number of
deaths occurs mainly because of population changes (size
and age group). In terms of risk, an increase in risk
is predicted for penile and anal cancers in men and
consequently an increase in mortality rates occurs
because of these types of cancers, in contrast to what is
expected for HPV-related cancers for women.
The reduction in mortality rates for women as well as in
the predictions for cervical, anal, vulvar, and vaginal
cancers probably occurred because of the measures
adopted to prevent cervical cancer. In Brazil, cytological
tracking for cervical cancer was started in the late 1950s,
but not as a collective action (Wunsch Filho and Moncau,
2002). In 1983, The Health Ministry attempted to
consolidate a health assistance service for women that
would allow access to the preventive cervical smear test.
However, most assistance was restricted to prenatal care.
Only in 1997 were the preventive measures effective at a
collective level, with the National Program for Cervical
Cancer Combat focusing on women between 25 and 59
years of age (Silva, 2004). A study that analyzed the
mortality trends of all cancers and 24 major cancer sites in
Brazil, using the WHO database along with Joinpoint
regression, observed a decrease in mortality because of
cervical cancer in the period 1980–2004 (Chatenoud et al.,
2010).
Corroborating the results presented here, a study on
cancer mortality in the European Union between 1970
and 2003 found a progressive reduction in cervical cancer
mortality, mainly among young and middle-aged women.
The study did not differentiate between cervical and
endometrial cancers, although the main reason provided
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Mortality trends and prediction of HPV-related cancers de Souza et al. 7
Table 3 Changes in the annual number of deaths between 2006–2010 and 2021–2025 and relative changes because of population size
and age structure, by site and sex, in Brazil
Change because of
Change in annual number [N (%)]
Men
Penile
Anal
Oropharyngeal
Total
Women
Cervical
Vulvar and vaginal
Anal
Oropharyngeal
Total
Risk (%)
Population (%)
1014
261
2577
3985
(65%)
(62%)
(31%)
(39%)
13
10
– 22
– 14
52
52
53
53
5717
890
259
915
7147
(24%)
(45%)
(32%)
(61%)
(25%)
– 25
– 17
– 28
1
– 26
49
62
60
60
51
by the authors for the reduction in rates was the
implementation of screening programs (Bosetti et al.,
2008); researches in other populations also corroborate
these results (Li et al., 2000; Canfell et al., 2006).
The reduction in mortality rates observed in women and
their increase in men are probably a result of differences
in health-related politics by sex in the country. Historically, preventive and assistance measures were a privilege
of women. Only in 2007 was there a focus on men’s health
in the national health scenario, and the results are still
incipient (Carrara et al., 2009).
The increase in HPV infection has led to the inclusion of
the vaccine as a public health measure in several
developed countries (De Vuyst et al., 2009; Bastos et al.,
2010). Immunization is essential for the reduction of
HPV-related cancers. Currently, vaccination is restricted
to women and it is argued that this protects men
indirectly. However, extension of immunization to men
must be considered with a focus on direct prevention of
HPV-related illnesses (Palefsky, 2010). Although the
efficacy of immunization has been shown, in Brazil, the
HPV vaccine has not been adopted by the government
and this action would definitely reduce the incidence of
cancer. Consequently, the decreasing trend observed in
HPV-related cancers in women would be even higher and
the increasing trend observed in mortality rates for penile
and anal cancers in men could be reverted.
The main limitation of our study is that trend analysis
and mortality predictions were carried out for the group
of cancers that could be associated with HPV. Nevertheless, not all the cancers studied have HPV as a
determining factor, such as oropharyngeal cancer, which
presents tobacco and alcohol as the main risk factors. The
results could be limited according to the prevalence of
HPV in the tumors for each location. However, evidence
of prevalence in Brazil is inconclusive and, because of its
great territorial extension and pronounced social and
regional differences, the generalization of prevalence
estimations could overestimate or underestimate the
results.
Data obtained in cancer mortality predictions must be
analyzed with care, always considering that they were
calculated on the basis of past trends, which may not
necessarily continue in the future. The greatest benefit
of trend and prediction analyses is that they lend support
to public health planning, through risk factor control,
immunization of populations to prevent infections related
to cancer, and screening programs, capable of modifying,
in the long term, the magnitude of the illness in the
population.
Acknowledgements
Conflicts of interest
There are no conflicts of interest.
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