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Epidemiological study of penile cancer in Pernambuco: experience of two reference centers

Abstract

Objectives

To investigate and analyze the epidemiological profile of penile cancer in the state of Pernambuco and compare this information with other studies related to the issue.

Material and Methods

We conducted a retrospective, observational and descriptive study of all patients with penile cancer in two reference centers in Pernambuco - Brazil, from 2007 to 2012. The variables studied were: age, region from the state, socio-economic situation, previous postectomy, smoking, time from the beginning of injury to diagnosis, staging of the primary lesion, tumor differentiation, treatment performed and death due to cancer.

Results

The total number of patients was 88. The highest prevalence was seen in those aged between 66 and 75 years. About the socio-economic situation, 67% worked informally and 64.8% received up to two minimum wages. Of all patients, 57% were married and 50% illiterate. The Metropolitan Region of Recife was the one with the highest number of cases, 41%. Tobacco smoking was reported in 48.9% of cases and prior postectomy in 3.4%. Most often it was observed an average period of six months from the onset of symptoms to diagnosis. And when the lesion was diagnosed, it usually had 2 to 5 cm (64.7%), stage T2 in 50% and well differentiated in 79.6%. Partial penectomy was performed in 76.1% and total in 17%. Death was observed in 27.3%.

Conclusion

The clinical profile and epidemiological characteristics found in this study are similar to other national and international studies related to the issue, i.e., typical of underdeveloped or developing countries.

penile cancer; epidemiology


INTRODUCTION

Penile cancer (PC) is a rare observed tumor in developed countries in North America and Europe. In the USA, the incidence is 0.2/100,000 inhabitants (1Burgers JK, Badalament RA, Drago JR. Penile cancer. Clinical presentation, diagnosis, and staging. Urol Clin North Am. 1992;19:247-56.); in Spain, the incidence is between 0.7 and 1.5/100,000 (2Ferrándiz-Pulido C, de Torres I, García-Patos V. Penile squamous cell carcinoma. Actas Dermosifiliogr. 2012;103:478-87.).

However, in many countries of Africa, South America and Asia, the disease represents an important health issue. Most cases in the world occur in India, Brazil and Uganda, with an incidence four (3Bleeker MC, Heideman DA, Snijders PJ, Horenblas S, Dillner J, Meijer CJ. Penile cancer: epidemiology, pathogenesis and prevention. World J Urol. 2009;27:141-50.) to six (1Burgers JK, Badalament RA, Drago JR. Penile cancer. Clinical presentation, diagnosis, and staging. Urol Clin North Am. 1992;19:247-56.) times higher than the above developed countries.

In Brazil, the highest incidences occur in North and Northeast regions, where most penile amputations are performed (4Brumini R: Câncer do Brasil: dados histopatológicos 1976-1980. Ministério da Saúde. Rio de Janeiro.; 1982.). However, there are very few epidemiological studies in the country in order to categorize that affected population.

The main objective of the present work is to evaluate the epidemiological and clinical characteristics of penile cancer in the state of Pernambuco (Brazil) in order to gather information about the disease in this region and to compare these data with other published in literature.

MATERIALS AND METHODS

This is a retrospective, observational, descriptive study, performed in the first semester of 2013. The data of the medical records of PC patients from Hospital do Cancer de Pernambuco (HCP) and Hospital Getulio Vargas (HGV) were reviewed. These are reference centers for this disease in the state. The reviewed data were from patients attended from January 2007 to December 2012. These hospitals are located in the city of Recife, capital of the Pernambuco State, situated in the Northeastern region of Brazil. Four patients were excluded: two from the state of Paraiba and two from the state of Alagoas.

The studied variables included: age, region of the state, marital status, work status, degree of education, socio-economic status, previous postectomy, smoking, period from the beginning of lesion until diagnosis, staging of primary lesion (TNM 2010), tumor differentiation, treatment performed, presence and localization of tumor recurrence, treatment of tumor recurrence and death due to PC.

The research was approved by the Ethical Committee of Federal University of Pernambuco.

RESULTS

Eighty-eight charts were reviewed, 76 from HCP and 12 from HGC. In 2010, according to the Brazilian Institute of Geography and Statistics, male population of Pernambuco state was 4,229,897, and penile cancer incidence was 2.08/100,000. Median age of patients was 61.2 years (±12.57) and the highest prevalence was observed in those with 66 to 75 years (25% of total) (Figure-1).

Figure 1
Geographic distribution of penile cancer in Pernambuco.

In relation to marital status, 57% were married, 33% single and 10% Widower.

Most had an informal job (67%), 25% had a formal work and 8% were unemployed. 23.8% had an income of less than a minimum wage (MW), 64.8% one to two MW and 11.4% three to four.

Fifty percent of patients were illiterate, 43.2% studied only until first grade and 6.8% attended high school.

Figure-2 shows that the metropolitan region of Recife was the region of the state that presented most cases. 48.9% of patients smoked and 3.7% were submitted to a previous postectomy.

Figure 2
Number of cases of penile cancer according to age.

In 68.1% of charts there was no information about the period between the initial symptoms and diagnosis. Among those with these data, 39.2% were diagnosed by biopsy of penile lesion that was performed up to six months from the beginning of symptoms, 25% after 7 to 11 months and 35.7% after one or more years.

Tumor size at diagnosis was less than 2 cm in 11 patients (12.5%), 2-5 cm in 57 patients (64.8%) and more than 2 cm in 20 patients (22.7%). Most patients presented T1 or T2 stages (36.4% and 50%, respectively – Table-1); 68.1% were N0 and 31.9% had positive lymph nodes. No distant metastasis was observed. 79.6% of lesions were well differentiated, 13.6% moderately differentiated, 5.7% undifferentiated and 1.1% sarcomatoid.

Table 1
Staging of penile cancer patients.

Surgical treatment is presented in Table-2. Adjuvant chemotherapy (AC) was performed in three cases. Four patients received palliative radiotherapy (RT). CT and RT were associated in two patients.

Table 2
Treatment.

Six patients received only clinical treatment (terminal patients).

PC relapsed in 28 patients (31.8%), 56% locally and 46.4% inguinal. Recurred lesions were treated according to Table-3.

Table 3
Treatment after tumoral recurrence.

Death occurred in 24 patients (27.3%) but it was not possible to stablish cancer-related death by other causes.

DISCUSSION

PC is the fourth most common tumor in men, after prostate, bladder and kidney cancers; it represents 2% of all malignant tumors of men, and caused 363 deaths in 2010 in Brazil (5Instituto Nacional de Câncer (Brasil). Coordenação de Prevenção e Vigilância. Câncer no Brasil: dados dos registros de base populacional, v. 4 / Rio de Janeiro: INCA, 2010.).

Frequency is variable, according to the analyzed region. In Brazil, the most frequently mentioned paper about PC epidemiology is the Brumini’s et al. work (4Brumini R: Câncer do Brasil: dados histopatológicos 1976-1980. Ministério da Saúde. Rio de Janeiro.; 1982.), that states that the higher incidence is observed in the northeast (5.7%) and north regions (5.3%). But this is a study performed in 1982 with data from 1976 to 1980. Favorito et al. (6Nardi AC, Glina S, Favorito LA. Epidemiological study of penile cancer in Brazil. Int Braz J Urol. 2007;33(Suppl 1):1-7.) related a higher description of cases in the Southeast region (45.54%), in particular in the state of São Paulo. This fact can be explained due to the higher economic power of that state, to where most cases migrate in order to search for treatment, in particular from the north and northeast regions.

This same dynamics is observed in the state of Pernambuco, where it was observed the highest incidence of PC in the metropolitan area of Recife. The higher economic status of the capital attracts several people from other regions, in search for work and better living conditions with better medical care, allowing for more precise diagnosis and treatments. The same aspects are observed in studies performed in the metropolitan regions of Salvador, capital of Bahia state (7Barbosa Júnior Ade A, Athanázio PR, Oliveira B. Cancer of the penis: study of its geographic pathology in the State of Bahia, Brazil. Rev Saude Publica. 1984;18:429-35.), and Belem, capital of Pará state (8Fonseca AG. Estudo epidemiológico do câncer de pênis no Estado do Pará, Brasil. Rev Pan-Amaz Saude. 2010;1:85-90.).

The incidence of PC in the Pará study was 5.7/100,000 inhabitants (8Fonseca AG. Estudo epidemiológico do câncer de pênis no Estado do Pará, Brasil. Rev Pan-Amaz Saude. 2010;1:85-90.), higher than the present series, 2.08/100.000 inhabitants. But this figure is underestimated, since there are others hospitals than these two reference centers in the region with more cases. Even so, the incidence is higher than that of Jews (9Barnholtz-Sloan JS, Maldonado JL, Pow-sang J, Giuliano AR. Incidence trends in primary malignant penile cancer. Urol Oncol. 2007;25:361-7. Erratum in: Urol Oncol. 2008;26:112. Guiliano, Anna R [corrected to Giuliano, Anna R].), North Americans (9Barnholtz-Sloan JS, Maldonado JL, Pow-sang J, Giuliano AR. Incidence trends in primary malignant penile cancer. Urol Oncol. 2007;25:361-7. Erratum in: Urol Oncol. 2008;26:112. Guiliano, Anna R [corrected to Giuliano, Anna R].) and Europeans (2Ferrándiz-Pulido C, de Torres I, García-Patos V. Penile squamous cell carcinoma. Actas Dermosifiliogr. 2012;103:478-87.).

The higher prevalence of the disease was observed in the sixth and seventh decades of life, similar to other national studies (6Nardi AC, Glina S, Favorito LA. Epidemiological study of penile cancer in Brazil. Int Braz J Urol. 2007;33(Suppl 1):1-7.,8Fonseca AG. Estudo epidemiológico do câncer de pênis no Estado do Pará, Brasil. Rev Pan-Amaz Saude. 2010;1:85-90.) and the world (2Ferrándiz-Pulido C, de Torres I, García-Patos V. Penile squamous cell carcinoma. Actas Dermosifiliogr. 2012;103:478-87.,1010 Hernandez BY, Barnholtz-Sloan J, German RR, Giuliano A, Goodman MT, King JB, Negoita S, Villalon-Gomez JM. Burden of invasive squamous cell carcinoma of the penis in the United States, 1998-2003. Cancer. 2008;113(10 Suppl):2883-91.,1111 Hegarty PK, Kayes O, Freeman A, Christopher N, Ralph DJ, Minhas S. A prospective study of 100 cases of penile cancer managed according to European Association of Urology guidelines. BJU Int. 2006;98:526-31.). It was also observed a significant amount of PC cases in young adults, with less than 45 years old (13.6%), what was worrying, since mutilation was performed in fully sexual active men.

Frisch et al. (1212 Frisch M, Friis S, Kjaer SK, Melbye M. Falling incidence of penis cancer in an uncircumcised population (Denmark 1943-90). BMJ. 1995;311:1471.) described three risk factors for the development of PC: phimosis/long foreskin, low social economic status and bad local hygiene. These factors are coincident with our results: most patients had an informal job (67%), with income lower than two minimum wages and many were illiterates (50%). Most studied patients had a bad cultural status, with compromised personal hygiene, with high risk sexual behavior (unprotected sexual relations, promiscuity) and exposition to sexually transmitted diseases (HPV) that could be related to PC (1313 Scheiner MA, Campos MM, Ornellas AA, Chin EW, Ornellas MH, Andrada-Serpa MJ. Human papillomavirus and penile cancers in Rio de Janeiro, Brazil: HPV typing and clinical features. Int Braz J Urol. 2008;34:467-74; discussion 475-6.). It is also important to stress the habitus of zoophilia, common in interior regions of the country, increasing the chance of PC occurrence, as related by Zequi et al. (1414 Zequi S de C, Guimarães GC, da Fonseca FP, Ferreira U, de Matheus WE, Reis LO, et al. Sex with animals (SWA): behavioral characteristics and possible association with penile cancer. A multicenter study. J Sex Med. 2012;9:1860-7.). This aspect was not analyzed in our series since it was not possible to obtain this information in the reviewed charts.

Phimosis/long foreskin, mentioned by Frisch (1212 Frisch M, Friis S, Kjaer SK, Melbye M. Falling incidence of penis cancer in an uncircumcised population (Denmark 1943-90). BMJ. 1995;311:1471.), could be present in 96.6% of patients, since only 3.4% had been previously submitted to postectomy. These features could lead to smegma accumulation and chronical inflammation, precursor to PC (1515 Plaut A, Kohn-Speyer AC. The Carcinogenic Action of Smegma. Science. 1947;105:391-2.). Circumcision, as observed in Jews, has a preventive role, when performed after birth (1616 Barnholtz-Sloan JS, Maldonado JL, Pow-sang J, Giuliano AR. Incidence trends in primary malignant penile cancer. Urol Oncol. 2007;25:361-7. Erratum in: Urol Oncol. 2008;26:112. Guiliano, Anna R [corrected to Giuliano, Anna R].); Maden et al. (1717 Maden C, Sherman KJ, Beckmann AM, Hislop TG, Teh CZ, Ashley RL, Daling JR. History of circumcision, medical conditions, and sexual activity and risk of penile cancer. J Natl Cancer Inst. 1993;85:19-24.) stated the incidence of PC is also lower when circumcision is performed in older children or adolescents, and in a recent study by Larke et al. (1818 Larke NL, Thomas SL, dos Santos Silva I, Weiss HA. Male circumcision and penile cancer: a systematic review and meta-analysis. Cancer Causes Control. 2011;22:1097-110.) it was proved that when circumcision is performed until 18 years of age it also protects against invasive PC.

Dodge et al. (1919 Dodge OG, Linsell CA. Carcinoma of the penis in Uganda and Kenya Africans. Cancer. 1963;16:1255-63.) compared Uganda and Kenya, neighbor countries located in Eastern Africa, with similar geopolitical and socio-cultural aspects. But the Kenyans usually submit (due to cultural and religious causes) their adolescents to circumcision, in a ritual of passage from childhood to adult life; only the minority muslin Ugandans are routinely circumcised. The procedure affects directly the incidence of PC in these countries; in Kenya, the incidence is 1.9% of all neoplasms and 7.15% in Uganda, being in this country the most common cancer in men.

On the other hand, in Scandinavia it is not culturally usual to perform circumcision and even so, the incidence of PC is very low, probably to good cultural status and personal hygiene, including the low income population (1212 Frisch M, Friis S, Kjaer SK, Melbye M. Falling incidence of penis cancer in an uncircumcised population (Denmark 1943-90). BMJ. 1995;311:1471.). According to this, it is possible to wonder which would be the most efficient method of prevention for our population: better hygiene awareness or routine circumcision for high risk groups. It is important to stress the presence of surgical complication after circumcision and the benefits and risks, and these measures should be studied by health care providers.

Among all studied patients, 58% were married and 51% of these had PC at T1 phase, in accordance to Rippentrop et al. (2020 Rippentrop JM, Joslyn SA, Konety BR. Squamous cell carcinoma of the penis: evaluation of data from the surveillance, epidemiology, and end results program. Cancer. 2004;101:1357-63.), that stated that married men presented with more precocious disease, probably due to spouse stimulus to seek for health care.

60.7% of patients waited more than 7 months to be diagnosed with PC, in accordance to the Kenyan study (2121 Magoha GA, Ngumi ZW. Cancer of the penis at Kenyatta National Hospital. East Afr Med J. 2000;77:526-30.), where more than 80% of patients were diagnosed after 6 months of symptoms, and to the Belem study (8Fonseca AG. Estudo epidemiológico do câncer de pênis no Estado do Pará, Brasil. Rev Pan-Amaz Saude. 2010;1:85-90.), where the patients waited for up to 11 months until diagnosis. This fact can be explained by ignorance, taboos, bad health care system, inappropriate treatments by uninformed physicians, delay to referral to urologists; these aspects are associated with late diagnosis and more advanced disease.

There was no significant relation between PC and smoking, as related by Harish et al (2222 Harish K, Ravi R. The role of tobacco in penile carcinoma. Br J Urol. 1995;75:375-7.); in our studied populations, smokers and non-smokers were equally present.

It was also observed that 63.6% of patients presented with more advanced disease (≥ T2) and 87.5% with lesion > 2 cm. These results are similar to a Brazilian epidemiological study of PC (6Nardi AC, Glina S, Favorito LA. Epidemiological study of penile cancer in Brazil. Int Braz J Urol. 2007;33(Suppl 1):1-7.), in a study performed in the state of Pará (8Fonseca AG. Estudo epidemiológico do câncer de pênis no Estado do Pará, Brasil. Rev Pan-Amaz Saude. 2010;1:85-90.) and in the Kenyan study (2121 Magoha GA, Ngumi ZW. Cancer of the penis at Kenyatta National Hospital. East Afr Med J. 2000;77:526-30.). And different from the North American study (1010 Hernandez BY, Barnholtz-Sloan J, German RR, Giuliano A, Goodman MT, King JB, Negoita S, Villalon-Gomez JM. Burden of invasive squamous cell carcinoma of the penis in the United States, 1998-2003. Cancer. 2008;113(10 Suppl):2883-91.), where 62.4% of patients were diagnosed in the initial and localized phases. The bigger the lesion and the more invasive, the higher is the possibility of lymph node involvement and worse prognosis (2323 Solsona E, Iborra I, Rubio J, Casanova JL, Ricós JV, Calabuig C. Prospective validation of the association of local tumor stage and grade as a predictive factor for occult lymph node micrometastasis in patients with penile carcinoma and clinically negative inguinal lymph nodes. J Urol. 2001;165:1506-9.).

Tumor differentiation had the same characteristics of other papers (8Fonseca AG. Estudo epidemiológico do câncer de pênis no Estado do Pará, Brasil. Rev Pan-Amaz Saude. 2010;1:85-90.,2121 Magoha GA, Ngumi ZW. Cancer of the penis at Kenyatta National Hospital. East Afr Med J. 2000;77:526-30.), being well differentiated carcinoma the most common observed tumor (Figure-3).

Figure 3
Tumor differentiation.

Most patients were submitted to penile amputation in some degree, reflecting the advanced characteristic of the disease.

Adjuvant chemotherapy and palliative radiotherapy, isolated or combined, were used in nine patients. Different treatments were performed in similar clinical settings. These facts reflect the lack of standardization of the treatment of penile cancer nowadays, particularly in relation to lymph node involvement (2424 Heyns CF, Fleshner N, Sangar V, Schlenker B, Yuvaraja TB, van Poppel H. Management of the lymph nodes in penile cancer. Urology. 2010;76(2 Suppl 1):S43-57.

25 Kroon BK, Horenblas S, Lont AP, Tanis PJ, Gallee MP, Nieweg OE. Patients with penile carcinoma benefit from immediate resection of clinically occult lymph node metastases. J Urol. 2005;173:816-9.

26 Cabanas RM. An approach for the treatment of penile carcinoma. Cancer. 1977;39:456-66.
-2727 Ornellas AA, Tobias-Machado M. Inguinal lymphadenectomy in penile cancer. Int Braz J Urol. 2007;33(Suppl 1):41-54.).

Another aspect is that, even in the presence of relatively easy diagnosis, many patients seek treatment in a stage beyond any possibility of treatment, representing 7% of our series. This fact is in accordance to the Kenyan study (2020 Rippentrop JM, Joslyn SA, Konety BR. Squamous cell carcinoma of the penis: evaluation of data from the surveillance, epidemiology, and end results program. Cancer. 2004;101:1357-63.) (9%) in 2000 and to the Salvador-Bahia study (7Barbosa Júnior Ade A, Athanázio PR, Oliveira B. Cancer of the penis: study of its geographic pathology in the State of Bahia, Brazil. Rev Saude Publica. 1984;18:429-35.) (7.3%) in 1984, probably due to the same previously described factors: ignorance, low cultural status, taboos, bad hygiene, etc.

Death occurred in 24 studied patients, but it was not possible to determine the cause of death, if due to PC. Probably this figure is underestimated since many patients lost follow-up and do not report death due to this neoplasm. Mutilation and death related to penile cancer are frequent, affecting self-esteem, causing psychological damage to the patients and to their families.

It is important that health care providers and politicians be aware of this disease, performing campaigns for orientation about this tumor, since it is not a very well-known disease by general population. It is important to stress the need of good hygiene practices, circumcision counseling and to provide good health care access. HPV vaccine can be an alternative for PC prevention but more studies are necessary in order to determine its role. With these measures, there will be a reduction of public health expenses, mutilations and related deaths.

CONCLUSIONS

Epidemiological and clinical aspects of PC in this series are similar to those of other Brazilian (6Nardi AC, Glina S, Favorito LA. Epidemiological study of penile cancer in Brazil. Int Braz J Urol. 2007;33(Suppl 1):1-7.,8Fonseca AG. Estudo epidemiológico do câncer de pênis no Estado do Pará, Brasil. Rev Pan-Amaz Saude. 2010;1:85-90.) and international series (1919 Dodge OG, Linsell CA. Carcinoma of the penis in Uganda and Kenya Africans. Cancer. 1963;16:1255-63.,2121 Magoha GA, Ngumi ZW. Cancer of the penis at Kenyatta National Hospital. East Afr Med J. 2000;77:526-30.), typical of underdeveloped or developing countries. Better prevention strategies and standardization of treatment are needed in order to reduce the incidence of PC.

REFERENCES

  • 1
    Burgers JK, Badalament RA, Drago JR. Penile cancer. Clinical presentation, diagnosis, and staging. Urol Clin North Am. 1992;19:247-56.
  • 2
    Ferrándiz-Pulido C, de Torres I, García-Patos V. Penile squamous cell carcinoma. Actas Dermosifiliogr. 2012;103:478-87.
  • 3
    Bleeker MC, Heideman DA, Snijders PJ, Horenblas S, Dillner J, Meijer CJ. Penile cancer: epidemiology, pathogenesis and prevention. World J Urol. 2009;27:141-50.
  • 4
    Brumini R: Câncer do Brasil: dados histopatológicos 1976-1980. Ministério da Saúde. Rio de Janeiro.; 1982.
  • 5
    Instituto Nacional de Câncer (Brasil). Coordenação de Prevenção e Vigilância. Câncer no Brasil: dados dos registros de base populacional, v. 4 / Rio de Janeiro: INCA, 2010.
  • 6
    Nardi AC, Glina S, Favorito LA. Epidemiological study of penile cancer in Brazil. Int Braz J Urol. 2007;33(Suppl 1):1-7.
  • 7
    Barbosa Júnior Ade A, Athanázio PR, Oliveira B. Cancer of the penis: study of its geographic pathology in the State of Bahia, Brazil. Rev Saude Publica. 1984;18:429-35.
  • 8
    Fonseca AG. Estudo epidemiológico do câncer de pênis no Estado do Pará, Brasil. Rev Pan-Amaz Saude. 2010;1:85-90.
  • 9
    Barnholtz-Sloan JS, Maldonado JL, Pow-sang J, Giuliano AR. Incidence trends in primary malignant penile cancer. Urol Oncol. 2007;25:361-7. Erratum in: Urol Oncol. 2008;26:112. Guiliano, Anna R [corrected to Giuliano, Anna R].
  • 10
    Hernandez BY, Barnholtz-Sloan J, German RR, Giuliano A, Goodman MT, King JB, Negoita S, Villalon-Gomez JM. Burden of invasive squamous cell carcinoma of the penis in the United States, 1998-2003. Cancer. 2008;113(10 Suppl):2883-91.
  • 11
    Hegarty PK, Kayes O, Freeman A, Christopher N, Ralph DJ, Minhas S. A prospective study of 100 cases of penile cancer managed according to European Association of Urology guidelines. BJU Int. 2006;98:526-31.
  • 12
    Frisch M, Friis S, Kjaer SK, Melbye M. Falling incidence of penis cancer in an uncircumcised population (Denmark 1943-90). BMJ. 1995;311:1471.
  • 13
    Scheiner MA, Campos MM, Ornellas AA, Chin EW, Ornellas MH, Andrada-Serpa MJ. Human papillomavirus and penile cancers in Rio de Janeiro, Brazil: HPV typing and clinical features. Int Braz J Urol. 2008;34:467-74; discussion 475-6.
  • 14
    Zequi S de C, Guimarães GC, da Fonseca FP, Ferreira U, de Matheus WE, Reis LO, et al. Sex with animals (SWA): behavioral characteristics and possible association with penile cancer. A multicenter study. J Sex Med. 2012;9:1860-7.
  • 15
    Plaut A, Kohn-Speyer AC. The Carcinogenic Action of Smegma. Science. 1947;105:391-2.
  • 16
    Barnholtz-Sloan JS, Maldonado JL, Pow-sang J, Giuliano AR. Incidence trends in primary malignant penile cancer. Urol Oncol. 2007;25:361-7. Erratum in: Urol Oncol. 2008;26:112. Guiliano, Anna R [corrected to Giuliano, Anna R].
  • 17
    Maden C, Sherman KJ, Beckmann AM, Hislop TG, Teh CZ, Ashley RL, Daling JR. History of circumcision, medical conditions, and sexual activity and risk of penile cancer. J Natl Cancer Inst. 1993;85:19-24.
  • 18
    Larke NL, Thomas SL, dos Santos Silva I, Weiss HA. Male circumcision and penile cancer: a systematic review and meta-analysis. Cancer Causes Control. 2011;22:1097-110.
  • 19
    Dodge OG, Linsell CA. Carcinoma of the penis in Uganda and Kenya Africans. Cancer. 1963;16:1255-63.
  • 20
    Rippentrop JM, Joslyn SA, Konety BR. Squamous cell carcinoma of the penis: evaluation of data from the surveillance, epidemiology, and end results program. Cancer. 2004;101:1357-63.
  • 21
    Magoha GA, Ngumi ZW. Cancer of the penis at Kenyatta National Hospital. East Afr Med J. 2000;77:526-30.
  • 22
    Harish K, Ravi R. The role of tobacco in penile carcinoma. Br J Urol. 1995;75:375-7.
  • 23
    Solsona E, Iborra I, Rubio J, Casanova JL, Ricós JV, Calabuig C. Prospective validation of the association of local tumor stage and grade as a predictive factor for occult lymph node micrometastasis in patients with penile carcinoma and clinically negative inguinal lymph nodes. J Urol. 2001;165:1506-9.
  • 24
    Heyns CF, Fleshner N, Sangar V, Schlenker B, Yuvaraja TB, van Poppel H. Management of the lymph nodes in penile cancer. Urology. 2010;76(2 Suppl 1):S43-57.
  • 25
    Kroon BK, Horenblas S, Lont AP, Tanis PJ, Gallee MP, Nieweg OE. Patients with penile carcinoma benefit from immediate resection of clinically occult lymph node metastases. J Urol. 2005;173:816-9.
  • 26
    Cabanas RM. An approach for the treatment of penile carcinoma. Cancer. 1977;39:456-66.
  • 27
    Ornellas AA, Tobias-Machado M. Inguinal lymphadenectomy in penile cancer. Int Braz J Urol. 2007;33(Suppl 1):41-54.
  • ABBREVIATIONS
    PC = Penile cancer
    TNM = Tumor – lymph node – metastasis - American Joint Committee on Cancer, 2010.
    HCP = Hospital do Câncer de Pernambuco
    HGV = Hospital Getúlio Vargas
    MW = minimum wage
    CT = chemotherapy
    RT = Radiotherapy
    HPV = Human papillomavirus

Publication Dates

  • Publication in this collection
    Dec 2014

History

  • Received
    12 Jan 2014
  • Accepted
    05 May 2014
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