Abstract
PURPOSE
This study aims to analyze the trends in mortality rates from penile cancer (PeC) and the treatment modalities adopted in Brazil over recent years.
MATERIALS AND METHODS
Death records for PeC cases (International Classification of Diseases, version 10 C60) and treatment modalities were extracted from the DATASUS database. A joinpoint regression analysis was conducted to examine the data.
RESULTS
A total of 7,848 deaths due to PeC were recorded in Brazil between 1996 and 2020. Increasing mortality trends were observed, with an average annual percentage change (AAPC) of 0.91 (0.6-1.2; P < .001). The North and Northeast regions had the highest age-standardized mortality rates (ASMRs) and AAPCs. From 2008 to 2020, the ASMR in the Northeast region remained stable, whereas the North region surpassed it. The Southeast region exhibited a significant downward trend, with an AAPC of –0.91 (–1.3 to -0.5; P < .001). Penile biopsies declined and were more frequent in the southeastern region. A total of 8,498 penile amputations were performed, with 39.4% and 29.1% conducted in the Southeast and Northeast regions, respectively.
CONCLUSION
Brazil has experienced increasing mortality trends in PeC over the past 2 decades. Low schooling, married, and young men from the North or Northeast regions represent the majority of deaths. Urgent efforts are needed to enhance the diagnosis and treatment of PeC to prevent and reduce mortality rates in the country.
Rising penile cancer deaths in Brazil, concentrated in North/Northeast. Interventions are needed, targeting disparities in education, marital status, and age. Regional insights guide health care strategies for improved outcomes.
INTRODUCTION
According to the 2020 Global Cancer Observatory (GLOBOCAN) estimates, there were 36,068 new cases of penile cancer (PeC) worldwide and 13,211 new deaths. Fifty-six percent occurred in Asia, with India reporting the highest percentage of cases. Latin America accounts for almost 14% of the new cases (4,988 cases), with 4.6% (1,658 cases) in Brazil. Asia had the highest number of deaths (8,189 cases) while Latin America registered 12.3% (1,627) of deaths.1
CONTEXT
Key Objective
What is the mortality profile of patients with penile cancer (PeC) in Brazil?
Knowledge Generated
This study examines regional trends and demographic characteristics, providing insights into this underexplored area of study. Brazil experienced an upward trend in PeC mortality. Deaths were predominantly among men with lower education, married status, and younger age, primarily concentrated in the Northern or Northeastern regions.
Relevance
Understanding these mortality trends and demographic patterns allows for tailored interventions and targeted health care strategies to address the disparities in PeC outcomes. Insights into regional variations provide crucial guidance for clinical and public health initiatives to improve diagnostic practices and timely interventions.
Brazil registered almost twice the incidence rate, in addition to a higher mortality rate than in global records. Between 2004 and 2014, the accumulated standardized incidence ratio was 6.15/100,000 in the Brazilian state of Maranhão.2
The carcinogenesis of PeC is multifactorial, with several risk factors, including poor hygiene, phimosis, chronic inflammation, multiple sexual partners, and a history of sexually transmitted diseases.3 Human papillomavirus (HPV) infection is also associated with PeC, being documented in 15%-80% of invasive cases and 70%-100% of intraepithelial lesions, particularly the subtypes 16 and 18.4,5
If diagnosed in early stages, PeC has a high potential of cure. Thereby, it is important to determine the mortality profile of diagnosed patients in Brazil. This study aimed to describe the profile of the patients died from PeC, the registered treatment modalities, and the time trends of mortality rates in Brazil over more than 2 decades.
MATERIALS AND METHODS
Data Source
In a recent study conducted by our group, we comprehensively examined the mortality trends of various urological cancers across different geographic regions in Brazil from 1996 to 2019.6 On the basis of this initial study, we reviewed the data retrieved from the DATASUS database of the Brazilian Public Health System (accessed on May 1, 2023). It was searched using the search code C60 from the International Classification of Diseases, version 10.7,8 We analyzed deaths from PeC between 1996-2020, besides the available information about the treatment modalities from 2008 to 2022.
The following variables were obtained from the mortality database: year of death, unit and region of the federation, place of residence, age, marital status, education level, and ethnicity. Patients were classified into the following age groups: 0-4, 5-9, 10-14, 15-19, 20-29, 30-39, 40-49, 50-59, 60-69, 70-79, and ≥80 years. For treatment information, the procedures associated with PeC were searched by nosocomial and outpatient production in the Hospital Information System and the Outpatient Information System. Both are components of the DATASUS database.9,10
The in-hospital procedures were searched by the surgical production, including penile amputation (code: 0416010016) between 2008 and 2022 and enlarged total penile amputation (code: 0416010229) from 2013 to 2022, because of the availability of data only in this period. The data were consolidated with respect to hospitalization and place of residence since 2008.
The outpatient procedures included chemotherapy for advanced PeC (code: 0304020370), penile biopsy (code: 0201010380), and penile radiation therapy (code: 0304010448) over the specified period.
Population data were obtained from the Brazilian Institute of Geography and Statistics for the Census conducted in 2000 and 2010. For the intercensus years, estimates and projections published by the same data source were used.8 Deaths with missing age information were excluded from the analyses.
Study Design
Geographic and temporal patterns were examined using age-standardized mortality rates (ASMRs), expressed as per 100,000 persons per year. Adjustment by age was performed by the direct method, using the world standard population created by Segi in 1960 and modified by Doll in 1966 11 as a reference for Brazil and the five geographic regions as follows: North (N), Northeast (NE), Central-West (CW), Southeast (SE), and South (S).
The two codes, 0416010229 and 0416010016, in the DATASUS system represent different procedures for penile amputation in oncology. Code 0416010229 refers to an extended total penile amputation, involving the removal of the entire penis and potentially including surrounding tissues and structures in complex cases. Conversely, code 0416010016 represents a standard penile amputation, involving the removal of the affected penile organ without additional extension. These codes serve as classification tools, allowing for differentiation on the basis of the scope and complexity of penile amputation procedures in an oncology setting.
Statistical Analyses
The Joinpoint Regression Program for Windows, version 4.8.0.1 (National Cancer Institute, Bethesda, MD; available at Surveillance Research Program12) was used to perform a joinpoint regression model to identify changes in mortality trends. The simplest joinpoint model was selected for the data allowed (maximum of four joinpoints). On the basis of this fitted model, the average annual percentage change (AAPC) was calculated for each region.13 The AAPC values were tested for equality to zero using the corresponding standard errors, and the values were considered statistically significant at P ≤ .05.
RESULTS
Between 1996 and 2020, 7,848 deaths due to PeC were registered in Brazil. Table 1 presents the patients' sociodemographic profile. Overall, 44% of deaths were in White male patients while 38.4%, in multiracial ethnicity. Regarding education, 20.2% of deaths occurred in illiterate patients, and more than 22% of deaths occurred in patients with up to 3 years of study. Considering the primary education, more than half of the deaths occurred in this level. In terms of marital status, 48.5% of the deaths were in married patients. With regard to age, 3,401 (43.3%) deaths were in men younger than 60 years, 1,693 (21.6%) in the group of 60-69 years, 1,451 (18.5%) in the group of 70-79 years, and 1,289 (16.4%) in men 80 years or older.
TABLE 1.
Demographic Characteristics of Penile Cancer–Related Deaths in Brazil (1996-2020)
| Variable | Brazil | North | Northeast | Central-West | Southeast | South |
|---|---|---|---|---|---|---|
| Marital status | ||||||
| Single | 2,007 (25.6) | 228 (34.9) | 708 (27.8) | 150 (23.9) | 755 (25.6) | 166 (15.5) |
| Married | 3,812 (48.6) | 257 (39.3) | 1,186 (46.5) | 299 (47.7) | 1,459 (49.5) | 611 (57) |
| Widower | 851 (10.8) | 55 (8.4) | 236 (9.3) | 63 (10) | 338 (11.5) | 159 (14.8) |
| Divorced | 371 (4.7) | 16 (2.4) | 74 (2.9) | 31 (4.9) | 182 (6.2) | 68 (6.3) |
| Others | 274 (3.5) | 43 (6.6) | 130 (5.1) | 29 (4.6) | 51 (1.7) | 21 (2) |
| Ignored | 533 (6.8) | 55 (8.4) | 215 (8.4) | 55 (8.8) | 162 (5.5) | 46 (4.3) |
| Total | 7,848 | 654 | 2,549 | 627 | 2,947 | 1,071 |
| Years of education | ||||||
| Illiterate | 1,575 (20.2) | 169 (25.9) | 787 (31) | 122 (19.6) | 357 (12.2) | 140 (13.3) |
| 1-3 years | 1,749 (22.4) | 174 (26.7) | 564 (22.2) | 138 (22.2) | 620 (21.1) | 253 (24) |
| 4-7 years | 1,384 (17.7) | 130 (19.9) | 304 (12) | 108 (17.3) | 570 (19.4) | 272 (25.9) |
| 8-11 years | 603 (7.7) | 55 (8.4) | 147 (5.8) | 43 (6.9) | 246 (8.4) | 112 (10.6) |
| 12+ years | 202 (2.6) | 12 (1.8) | 33 (1.3) | 19 (3) | 116 (4) | 22 (2.1) |
| Ignored | 2,335 (29.8) | 114 (17.4) | 714 (28) | 197 (31.4) | 1,038 (35.2) | 272 (25.4) |
| Total | 7,848 | 654 | 2,549 | 627 | 2,947 | 1,071 |
| Race | ||||||
| White | 3.462 (44.1) | 92 (14.1) | 580 (22.8) | 236 (37.6) | 1.666 (56.5) | 888 (82.9) |
| Black | 520 (6.6) | 23 (3.5) | 219 (8.6) | 53 (8.5) | 207 (7) | 18 (1.7) |
| Asian | 36 (0.5) | 2 (0.3) | 15 (0.6) | 1 (0.2) | 17 (0.6) | 1 (0.1) |
| Multiracial | 3.010 (38.4) | 473 (72.3) | 1.450 (56.9) | 258 (41.1) | 746 (25.3) | 83 (7.7) |
| Indigenous | 36 (0.5) | 17 (2.6) | 6 (0.2) | 11 (1.8) | 2 (0.1) | 0 (0) |
| Ignored | 784 (10) | 47 (7.2) | 279 (10.9) | 68 (10.8) | 309 (10.5) | 81 (7.6) |
| Total | 7.848 | 654 | 2.549 | 627 | 2.947 | 1.071 |
| Age group, years | ||||||
| <49 | 1,817 (23.2) | 175 (26.8) | 631 (24.8) | 664 (22.5) | 181 (16.9) | 166 (26.5) |
| 50-59 | 1,584 (20.2) | 131 (20) | 491 (19.3) | 631 (21.4) | 201 (18.8) | 130 (20.7) |
| 60-69 | 1,693 (21.6) | 145 (22.2) | 499 (19.6) | 646 (21.9) | 266 (24.8) | 137 (21.9) |
| 70-79 | 1,451 (18.5) | 110 (16.8) | 445 (17.5) | 556 (18.9) | 228 (21.3) | 112 (17.9) |
| ≥80 | 1,289 (16.4) | 92 (14.1) | 477 (18.7) | 444 (15.1) | 195 (18.2) | 81 (12.9) |
| Ignored | 14 (0.2) | 1 (0.2) | 6 (0.2) | 6 (0.2) | 0 (0) | 1 (0.2) |
| Total | 7,848 | 654 | 2,549 | 2,947 | 1,071 | 627 |
NOTE. Numbers in parentheses are percentages.
In 2020, the Brazilian region with the highest ASMR was the N with 0.54 deaths per 100,000 men, followed by the NE, with 0.53/100,000 men. The lowest ASMR was in the SE region (Appendix Table A1). Considering the whole period, it was registered increasing mortality trends in Brazil, characterized by an AAPC of 0.91 (0.6-1.2; P < .001; Fig 1). North and NE regions exhibited the highest ASMRs and annual percentage changes (APCs) for PeC (Fig 2). Notably, in the period from 2008 to 2020, the ASMR in the NE region remained relatively constant (APC, 0.69 [95% CI, –0.6 to 2]; P = .293), and it was exceeded by the mortality in the North (Fig 2). A notable downward trend was solely identified in the Southeast region (AAPC, –0.91 [95% CI, –1.3 to –0.5]; P < .001).
FIG 1.
Trends in the age-standardized mortality rates for penile cancer in Brazil. APC, annual percentage change.
FIG 2.
Trends in the age-standardized mortality rates for penile cancer in the Brazilian regions. APC, annual percentage change.
The surgical procedures considered for the PeC diagnosis and treatment are shown in Figure 3. Penile biopsies declined annually. The highest number of penile biopsies was registered in the period from 2008 to 2010. After 2010, the number of biopsies sharply decreased in the NE region from more than a 1,000 procedures to an annual number below 200 biopsies. Overall, 8,498 penile amputations were performed over a 15-year period (2008-2022). Most of these procedures were performed in the SE region (39.4%), followed by the NE (29.1%; Appendix Table A2).
FIG 3.
Number of procedures related to penile cancer of Brazil, 2008-2022.
Our data revealed 15,609 cycles of chemotherapy between 2008 and 2022. The SE region had the highest percentage of chemotherapy treatments (35.1%), followed by the NE region (34.8%). The CW region had the lowest percentage of chemotherapy treatments (6.5%).
Radiotherapy was registered only from 2019 to 2022, with 553 procedures (9.8% in the N, 31.6% in the NE, 34.7% in the SE, 17.4% in the S, and 6.5% in the CW).
DISCUSSION
The findings of this study provide valuable insights into the current status of PeC mortality in Brazil, emphasizing several critical aspects that require attention. The analysis of mortality rates revealed that the N and the NE regions exhibited the highest mortality rates, demonstrating an increasing trend throughout the study period, particularly in the N region.
The decline in penile biopsies observed within these regions may be associated with these mortality trends. By contrast, the SE region recorded the highest number of penile biopsies and surgical procedures, distinguishing itself as the only region with a significant downward trend in mortality rates. Additionally, when evaluating the number of chemotherapy sessions over the study period, the SE region demonstrated similarities to the NE region, which reported lower rates of diagnostic biopsies and penile amputations. This finding suggests a potential association between these factors and the diagnosis of more advanced PeC cases in the NE region.
The mortality rates observed in the N, NE, and CW regions were notably high, bearing similarities to other regions across the globe. Specifically, these rates were comparable with those found in Eastern Africa (age-standardized rate [ASR], 0.58/100,000), South-Central Asia (ASR, 0.58/100,000), and the Caribbean (ASR, 0.45/100,000).1
Several risk factors have been previously identified for PeC, including phimosis, smoking, sexually transmitted infections, engaging in sexual activities with animals,14 and poor hygiene habits. These risk factors present opportunities for intervention and preventive measures. Notably, a systematic review highlighted the high prevalence of HPV in penile tumors (51%),15 underscoring the importance of initiatives aimed at reducing its prevalence. A study evaluating the efficacy of the quadrivalent HPV vaccine demonstrated a 65.5% of effectiveness in preventing HPV-related lesions.16
In response to the urgency of addressing this issue, the Brazilian Society of Urology (SBU) launched educational campaigns in 2006 and 2007, emphasizing the significance of adopting proper hygiene habits and promoting early diagnosis. The investigation period in our study began immediately after these campaigns, and initial improvements were observed, possibly attributed to increased awareness or coincidental factors. However, after 2009-2010, there was a decline in the number of biopsies conducted, accompanied by an increase in the number of amputations. Consequently, it is imperative to implement a sustained and comprehensive program that continuously raises public awareness and engages politicians and health authorities in combatting this devastating disease.
Penile biopsy is a relatively simple outpatient procedure that has been consistently declining since 2009. Several factors may contribute to this decline. First, health care practitioners in the primary care network, who play a crucial role in patient care, might lack the necessary training and resources for conducting biopsies and examining pathology, especially in regions with high incidence rates. Moreover, we acknowledge the possibility that an increasing number of cases with unequivocal clinical presentations are being directly referred to tertiary health care facilities, bypassing the biopsy stage. This bypass might stem from various factors, including limited access to specialized health care services, delayed referrals, or a lack of awareness among both patients and health care professionals regarding the critical role of early diagnosis through biopsies.
Additionally, educational campaigns targeting both health care providers and the general population are crucial to raising awareness about the significance of timely biopsies in diagnosing PeC and facilitating early intervention.
Access to specialized oncology health care facilities in Brazil is a critical component of addressing PeC. The country has established Centers of High Complexity Assistance in Oncology and Units of High Complexity Assistance in Oncology across all states, ensuring comprehensive and specialized care for patients with cancer. This network aims to provide diagnostic services, treatment options, and surgical interventions, thus facilitating accessible and quality care for individuals diagnosed with cancer, regardless of their geographic location within Brazil.
Our findings are consistent with the existing literature, which has demonstrated a correlation between higher mortality and amputation rates and regions/states with lower socioeconomic development.17,18 This relationship may have been further exacerbated by the recent economic crisis in Brazil. The impact of this crisis was particularly pronounced in Brazil between 2014 and 2019, coinciding with our study period.19
Furthermore, there is a well-established inverse association between the level of education and the incidence of PeC, with individuals who have lower levels of education being at a higher risk of diagnosis.20-22 A study conducted in Paraguay found that 91% of 103 patients had either no educational background or only completed primary education.4 Our study revealed that 60.3% of deaths by PeC occurred in men with only the primary level of education. When considered the N and the NE regions, these proportions are higher (72.5% and 65.2%, respectively, of men with lower than 8 years of education). It is likely that these patients face additional barriers in seeking timely and appropriate medical assistance.
According to the Continuous National Household Sample Survey (Continuous PNAD) conducted in 2018, the NE, N, and CW regions of Brazil exhibited the highest illiteracy rates of 13.9%.23 Notably, these regions corresponded to the areas with the highest PeC mortality rates in our study. By contrast, the regions with the lowest PeC mortality rates, namely the South and Southeast, had the highest literacy rates, at 3.6% and 3.5%, respectively. Patients with more than 12 years of education have a significantly lower percentage of deaths from PeC, particularly when compared with those with only primary education. This suggests that the high level of education may serve as a protective factor against mortality from PeC. Higher education levels are often associated with increased awareness of health risks, better access to health care services, and a greater likelihood of adopting preventive measures.
Furthermore, the SBU epidemiological study in 2008 reported that 21.2% of cases occurred in men age between 56 and 65 years. Our research demonstrated that deaths by PeC predominantly occurred in men younger than 60 years (43.4%), besides 21.6% between 60 and 69 years. Thus, our study unveils a concerning scenario for the aging population.
Interestingly, our study revealed that the majority of individuals who died were married, which differs from the characteristics observed in the study conducted by Mao et al.24 Mao et al evaluated the mortality of 3,195 patients from the SEER database and found that marital status was an independent prognostic factor for overall survival (OS) and cancer-specific survival, with widowed men exhibiting the worst outcomes in terms of both OS and cancer-specific survival. This raises the question of whether the higher mortality proportion in this group is due to factors such as increased support from family members who may encourage seeking medical attention or potentially better detection and reporting of cases. It is possible that unmarried individuals, particularly those without strong support networks, may be less likely to seek medical care or have their cases accurately recorded in official statistics, leading to underreporting.
This study presents several limitations that should be taken into consideration. First, the mortality data used are based on records from the Brazilian public health system, which may lead to underreporting or errors in the registration of deaths. However, it is important to note that PeC is a rare and chronic disease that predominantly affects the public health care system, reducing the likelihood of significant errors in the quality of mortality rates. Furthermore, the lack of socioeconomic resources among patients with PeC and the low utilization of private or supplementary health care services indicate that our findings likely reflect the mortality profile of the majority of invasive patients with PeC in Brazil. It is notably evident that certain regions, particularly the Northern region, displayed fluctuations in their ASMR. They could arise from diverse factors. Natural year-to-year variations might result from random fluctuations in data collection, alterations in reporting methods, or variations in the size of the at-risk population. Regions with fewer cases or less precise data collection methods could exhibit more notable year-to-year differences. Furthermore, specific regional influences, such as socioeconomic factors, unequal health care access, cultural disparities, or differing prevalence rates of PeC risk factors in the Northern region, might contribute to them.
Another limitation is that the analyzed data only pertain to mortality from PeC, without encompassing information on incidence, tumor staging, or the treatments used. Therefore, it was not possible to establish a direct relationship between treatment outcomes and mortality rates.
Additionally, it is important to acknowledge that the accurate interpretation and utilization of codes within the DATASUS system, including 0416010229 and 0416010016, are the responsibility of health care professionals. Although we used these codes as classification tools to differentiate penile amputation modalities on the basis of the scope and complexity of the procedures, there may be variations in the application of these codes among different institutions and health care practitioners.
Last, it is important to highlight that this study covered a period of over 2 decades. In this period, changes in clinical practice, health policies, and public awareness regarding PeC may have occurred. These factors could have influenced the observed patterns of mortality and should be considered when interpreting the results.
Despite these limitations, this study provides valuable insights into the mortality profile of PeC in Brazil and underscores the need for more effective prevention, early diagnosis, and treatment approaches to reduce the impact of this disease. Low schooling, married, and young men from the N or NE regions represent the majority of deaths from PeC. It is crucial to prioritize efforts in improving early diagnosis and biopsy. In this regard, engaging the medical community in initiatives aimed at enhancing penile biopsy rates becomes essential for improving overall outcomes and reducing mortality associated with this condition. A final opinion is to emphasize the importance of the HPV vaccination in both sexes as its effectiveness in preventing HPV-related lesions exceeds 50%-60%.
In conclusion, over the period, there were increasing mortality trends in Brazil. The N and NE regions had the highest ASMRs and AAPCs. Penile biopsies have declined in all the countries, and they were more frequently performed in the southeastern region. Low schooling, married, and young men from the N or NE regions represent the majority of deaths.
These findings provide an important database for implementing effective measures that ensure early diagnosis, enabling conservative treatments and facilitating the return of patients to their social activities. It is worth noting that there has been a surprising shift in mortality rates, with the N region surpassing the NE. This change emphasizes the dynamic nature of PeC mortality across different regions in Brazil, warranting targeted interventions in the N and NE regions to address the rising mortality rates effectively. Additionally, preventive measures, especially the expansion of HPV vaccination, should be emphasized.
APPENDIX
TABLE A1.
Age-Standardized Mortality Rates for Penile Cancer in Brazil and Brazilian Regions by Year (1996-2020)
| Year | Region | |||||
|---|---|---|---|---|---|---|
| Brazil | North | Northeast | Central-West | Southeast | South | |
| 1996 | 0.28 (0.24-0.33) | 0.12 (0.01-0.24) | 0.21 (0.14-0.29) | 0.53 (0.27-0.78) | 0.32 (0.25-0.39) | 0.26 (0.16-0.37) |
| 1997 | 0.33 (0.28-0.38) | 0.59 (0.32-0.86) | 0.23 (0.16-0.30) | 0.41 (0.19-0.62) | 0.34 (0.27-0.42) | 0.35 (0.23-0.47) |
| 1998 | 0.32 (0.27-0.36) | 0.16 (0.04-0.29) | 0.27 (0.19-0.35) | 0.59 (0.33-0.84) | 0.33 (0.26-0.40) | 0.32 (0.20-0.44) |
| 1999 | 0.34 (0.29-0.38) | 0.22 (0.05-0.38) | 0.35 (0.26-0.44) | 0.57 (0.31-0.83) | 0.30 (0.23-0.36) | 0.42 (0.28-0.55) |
| 2000 | 0.30 (0.26-0.34) | 0.17 (0.03-0.30) | 0.26 (0.19-0.34) | 0.41 (0.21-0.60) | 0.32 (0.26-0.39) | 0.33 (0.22-0.44) |
| 2001 | 0.30 (0.26-0.34) | 0.38 (0.18-0.58) | 0.31 (0.23-0.39) | 0.33 (0.15-0.51) | 0.30 (0.24-0.36) | 0.26 (0.16-0.35) |
| 2002 | 0.31 (0.27-0.36) | 0.30 (0.14-0.46) | 0.31 (0.23-0.39) | 0.37 (0.18-0.56) | 0.32 (0.26-0.39) | 0.29 (0.19-0.39) |
| 2003 | 0.33 (0.29-0.37) | 0.38 (0.19-0.57) | 0.29 (0.21-0.36) | 0.22 (0.08-0.36) | 0.37 (0.31-0.44) | 0.31 (0.21-0.42) |
| 2004 | 0.37 (0.33-0.42) | 0.34 (0.17-0.51) | 0.43 (0.34-0.53) | 0.35 (0.17-0.53) | 0.35 (0.28-0.41) | 0.38 (0.27-0.50) |
| 2005 | 0.33 (0.29-0.38) | 0.31 (0.15-0.47) | 0.39 (0.30-0.47) | 0.66 (0.42-0.91) | 0.29 (0.23-0.35) | 0.26 (0.16-0.35) |
| 2006 | 0.37 (0.33-0.42) | 0.35 (0.17-0.53) | 0.48 (0.38-0.58) | 0.56 (0.34-0.78) | 0.33 (0.27-0.40) | 0.25 (0.16-0.34) |
| 2007 | 0.35 (0.31-0.39) | 0.42 (0.23-0.60) | 0.42 (0.33-0.51) | 0.42 (0.24-0.60) | 0.28 (0.22-0.33) | 0.37 (0.27-0.47) |
| 2008 | 0.38 (0.33-0.42) | 0.60 (0.39-0.82) | 0.58 (0.48-0.68) | 0.38 (0.22-0.54) | 0.26 (0.21-0.31) | 0.30 (0.21-0.40) |
| 2009 | 0.34 (0.30-0.38) | 0.35 (0.19-0.51) | 0.45 (0.36-0.54) | 0.33 (0.18-0.48) | 0.30 (0.24-0.35) | 0.29 (0.20-0.38) |
| 2010 | 0.38 (0.34-0.42) | 0.37 (0.21-0.52) | 0.54 (0.44-0.63) | 0.51 (0.33-0.68) | 0.28 (0.23-0.33) | 0.36 (0.26-0.45) |
| 2011 | 0.35 (0.31-0.38) | 0.54 (0.35-0.73) | 0.47 (0.38-0.56) | 0.41 (0.25-0.57) | 0.27 (0.22-0.32) | 0.24 (0.16-0.32) |
| 2012 | 0.39 (0.35-0.43) | 0.60 (0.40-0.80) | 0.53 (0.44-0.62) | 0.51 (0.34-0.68) | 0.30 (0.25-0.36) | 0.25 (0.17-0.34) |
| 2013 | 0.39 (0.35-0.43) | 0.62 (0.42-0.82) | 0.53 (0.44-0.63) | 0.34 (0.21-0.48) | 0.32 (0.27-0.37) | 0.30 (0.21-0.38) |
| 2014 | 0.37 (0.34-0.41) | 0.68 (0.48-0.89) | 0.53 (0.44-0.62) | 0.46 (0.30-0.62) | 0.26 (0.22-0.31) | 0.30 (0.22-0.39) |
| 2015 | 0.38 (0.34-0.41) | 0.66 (0.46-0.87) | 0.47 (0.38-0.55) | 0.55 (0.38-0.72) | 0.29 (0.24-0.33) | 0.32 (0.24-0.40) |
| 2016 | 0.37 (0.33-0.40) | 0.74 (0.53-0.95) | 0.51 (0.42-0.59) | 0.36 (0.23-0.50) | 0.27 (0.23-0.32) | 0.30 (0.22-0.38) |
| 2017 | 0.39 (0.35-0.42) | 0.77 (0.56-0.98) | 0.55 (0.46-0.64) | 0.46 (0.31-0.61) | 0.27 (0.23-0.32) | 0.30 (0.22-0.38) |
| 2018 | 0.39 (0.35-0.42) | 0.58 (0.41-0.76) | 0.56 (0.48-0.65) | 0.50 (0.35-0.65) | 0.28 (0.23-0.32) | 0.30 (0.22-0.38) |
| 2019 | 0.38 (0.34-0.41) | 0.55 (0.38-0.72) | 0.56 (0.47-0.64) | 0.36 (0.23-0.48) | 0.28 (0.24-0.33) | 0.32 (0.24-0.39) |
| 2020 | 0.37 (0.33-0.40) | 0.54 (0.37-0.71) | 0.53 (0.45-0.61) | 0.31 (0.19-0.43) | 0.27 (0.22-0.31) | 0.39 (0.30-0.47) |
TABLE A2.
Number and Percentage of Penile Amputations in the Brazilian States Between 2008 and 2022
| Brazilian State | No. (%) |
|---|---|
| São Paulo | 1,412 (16.6) |
| Minas Gerais | 1,218 (14.3) |
| Paraná | 701 (8.2) |
| Ceará | 566 (6.7) |
| Rio de Janeiro | 484 (5.7) |
| Rio Grande do Sul | 444 (5.2) |
| Pernambuco | 429 (5.0) |
| Maranhão | 421 (5.0) |
| Pará | 419 (4.9) |
| Bahia | 360 (4.2) |
| Santa Catarina | 237 (2.8) |
| Espírito Santo | 233 (2.7) |
| Piauí | 229 (2.7) |
| Goiás | 216 (2.5) |
| Rio Grande do Norte | 207 (2.4) |
| Mato Grosso | 132 (1.6) |
| Amazonas | 127 (1.5) |
| Distrito Federal | 113 (1.3) |
| Paraíba | 99 (1.2) |
| Mato Grosso do Sul | 89 (1.0) |
| Tocantins | 82 (1.0) |
| Sergipe | 81 (1.0) |
| Alagoas | 79 (0.9) |
| Rondônia | 71 (0.8) |
| Roraima | 20 (0.2) |
| Amapá | 16 (0.2) |
| Acer | 13 (0.2) |
| Total | 8,498 (100) |
AUTHOR CONTRIBUTIONS
Conception and design: Thiago Camelo Mourão, Artur Agostinho Beraldi, Maria Paula Curado, Stênio de Cássio Zequi
Administrative support: Stênio de Cássio Zequi
Collection and assembly of data: Thiago Camelo Mourão, Plínio Ramos Pinto Neto, Rafael Valente Batista, Jayme Quirino Caon Nobre
Data analysis and interpretation: Thiago Camelo Mourão, Artur Agostinho Beraldi, Gisele Aparecida Fernandes, Maria Paula Curado
Manuscript writing: All authors
Final approval of manuscript: All authors
Accountable for all aspects of the work: All authors
AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST
The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated unless otherwise noted. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/go/authors/author-center.
Open Payments is a public database containing information reported by companies about payments made to US-licensed physicians (Open Payments).
Gisele Aparecida Fernandes
Employment: A.C. Camargo Cancer Center
Stênio de Cássio Zequi
Consulting or Advisory Role: Pfizer, Astellas Brazil
Speakers' Bureau: Pfizer, Astellas Pharma, Bayer, Janssen, AstraZeneca Brazil, MSD
No other potential conflicts of interest were reported.
REFERENCES
- 1.Ferlay J, Ervik M, Lam F, et al. : Global Cancer Observatory: Cancer Today. International Agency for Research on Cancer, 2020. https://gco.iarc.fr/today [Google Scholar]
- 2.Coelho RWP, Pinho JD, Moreno JS, et al. : Penile cancer in Maranhão, Northeast Brazil: The highest incidence globally? BMC Urol 18:50-57, 2018 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Kidd LC, Chaing S, Chipollini J, et al. : Relationship between human papillomavirus and penile cancer—implications for prevention and treatment. Transl Androl Urol 6:791-802, 2017 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Chaux A, Netto GJ, Rodríguez IM, et al. : Epidemiologic profile, sexual history, pathologic features, and human papillomavirus status of 103 patients with penile carcinoma. World J Urol 31:861-867, 2013 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Miralles-Guri C, Bruni L, Cubilla AL, et al. : Human papillomavirus prevalence and type distribution in penile carcinoma. J Clin Pathol 62:870-878, 2009 [DOI] [PubMed] [Google Scholar]
- 6.Mourão TC, Curado MP, de Oliveira RAR, et al. : Epidemiology of urological cancers in Brazil: Trends in mortality rates over more than two decades. J Epidemiol Glob Health 12:239-247, 2022 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.DATASUS. Department of Informatics. Ministry of Health, Brazil. Information in Health: Mortality Information System. http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sim/cnv/obt10uf.def [Google Scholar]
- 8.DATASUS. Department of Informatics. Ministry of Health, Brazil. Information in Health: Demographic and Socioeconomic. http://www2.datasus.gov.br/DATASUS/index.php?area=0206&id=6942 [Google Scholar]
- 9.DATASUS. Department of Informatics. Ministry of Health, Brazil. Outpatient Information System. http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sia/cnv/qauf.def [Google Scholar]
- 10.DATASUS. Department of Informatics. Ministry of Health, Brazil. Hospital Information System. http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sih/cnv/qiuf.def [Google Scholar]
- 11.Doll R, Cook P: Summarizing indices for comparison of cancer incidence data. Int J Cancer 2:269-279, 1967 [DOI] [PubMed] [Google Scholar]
- 12.National Cancer Institute: Joinpoint Regression Program, version 5.0.2. Statistical Methodology and Applications Branch, Survellience Research Program, 2023. https://surveillance.cancer.gov/joinpoint
- 13.Kim H-J, Fay MP, Feuer EJ, et al. : Permutation tests for joinpoint regression with applications to cancer rates. Stat Med 19:335-351, 2000 [DOI] [PubMed] [Google Scholar]
- 14.Zequi SdeC, Guimarães GC, da Fonseca FP, et al. : Sex with animals (SWA): Behavioral characteristics and possible association with penile cancer. A multicenter study. J Sex Med 9:1860-1867, 2012 [DOI] [PubMed] [Google Scholar]
- 15.Yu Y-B, Wang Y-H, Yang X-C, et al. : The relationship between human papillomavirus and penile cancer over the past decade: A systematic review and meta-analysis. Asian J Androl 21:375, 2019 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Giuliano AR, Palefsky JM, Goldstone S, et al. : Efficacy of quadrivalent HPV vaccine against HPV infection and disease in males. N Engl J Med 364:401-411, 2011 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.do Couto TC, Arruda RMB, do Couto MC, et al. : Epidemiological study of penile cancer in Pernambuco: Experience of two reference centers. Int Braz J Urol 40:738-744, 2014 [DOI] [PubMed] [Google Scholar]
- 18.da Fonseca AG, de A Pinto JAS, Marques MC, et al. : Estudo epidemiológico do câncer de pênis no Estado do Pará, Brasil. Rev Panamazonica Saude 1:85-90, 2010 [Google Scholar]
- 19.Drago HF, de Moura GL, Marchi J: A crise econômica mundial de 2008 e o reflexo sobre as instituições bancárias brasileiras. Revista Estudo Debate 24:26-41, 2017 [Google Scholar]
- 20.Sharma P, Zargar-Shoshtari K, Pettaway CA, et al. : Disparities in penile cancer. Cancer Control 23:409-414, 2016 [DOI] [PubMed] [Google Scholar]
- 21.Hernandez BY, Barnholtz-Sloan J, German RR, et al. : Burden of invasive squamous cell carcinoma of the penis in the United States, 1998-2003. Cancer 113:2883-2891, 2008 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Colón-López V, Ortiz AP, Soto-Salgado M, et al. : Penile cancer disparities in Puerto Rican men as compared to the United States population. Int Braz J Urol 38:728-738, 2012 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Instituto Brasileiro de Geografia e Estatística : Pesquisa Nacional por Amostra de Domicílios Contínua—PNAD. https://www.ibge.gov.br/estatisticas/sociais/educacao
- 24.Mao W, Zhang Z, Huang X, et al. : Marital status and survival in patients with penile cancer. J Cancer 10:2661-2669, 2019 [DOI] [PMC free article] [PubMed] [Google Scholar]