You are on page 1of 8

1

Sex with Animals (SWA): Behavioral Characteristics and Possible Association with Penile Cancer. A Multicenter Study
jsm_2512 1..8

Stnio de Cssio Zequi, PhD,* Gustavo Cardoso Guimares, PhD,* Francisco Paulo da Fonseca, PhD,* Ubirajara Ferreira, PhD, Wagner Eduardo de Matheus, PhD, Leonardo Oliveira Reis, MD, Giuliano Amorim Aita, MD, Sidney Glina, PhD, Victor Silvestre Soares Fanni, MD, Marjo Denisson Cardenuto Perez, PhD, Luiz Renato Montez Guidoni, MD, Valdemar Ortiz, PhD,** Lucas Nogueira, MD, Luis Carlos de Almeida Rocha, PhD, Gustavo Cuck, MD, Walter Henriques da Costa, MD, Ravendra Ryan Moniz, MD, Jos Hiplito Dantas Jr., MD,*** Fernando Augusto Soares, PhD, and Ademar Lopes, PhD*
*Urology Division of Pelvic Surgery Department, Hospital A C Camargo, So Paulo, SP, Brazil; Urology Division, UNICAMP Universidade Estadual de Campinas, Campinas, SP, Brazil; Urologic Department, Hospital So Marcus, Teresina, PI, Brazil; Urology Division, Hospital Ipiranga, So Paulo, SP, Brazil; Urology Division of Surgical Department FCMSCSP, Faculdade de Cincias Mdicas da Santa Casa de So Paulo, SP, Brazil; **Urology Department, UNIFESP, Universidade Federal de So Paulo, So Paulo, SP, Brazil; Urology Department, UFMG, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil; Urology Department, Hospital das Clnicas da UFPR, Universidade Federal do Paran, Curitiba, PR, Brazil; Urology Division, Hospital da Aeronutica de So Paulo, SP, Brazil; Urology Service, Hospital, Geral de Carapicuba, SP, Brazil; ***Genitourinary Diseases Disciplin, Hospital Universitrio Onofre Lopes, UFRN, Universidade Federal do Rio Grande do Norte, RN, Brazil; Surgical and Investigative Pathology Department, Hospital A C Camargo, So Paulo, SP, Brazil DOI: 10.1111/j.1743-6109.2011.02512.x

ABSTRACT

Introduction. Zoophilia has been known for a long time but, underreported in the medical literature, is likely a risk factor for human urological diseases. Aim. To investigate the behavioral characteristics of sex with animals (SWA) and its associations with penile cancer (PC) in a case-control study. Methods. A questionnaire about personal and sexual habits was completed in interviews of 118 PC patients and 374 controls (healthy men) recruited between 2009 and 2010 from 16 urology and oncology centers. Main Outcome Measures. SWA rates, geographic distribution, duration, frequency, animals involved, and behavioral habits were investigated and used to estimate the odds of SWA as a PC risk factor. Results. SWA was reported by 171 (34.8%) subjects, 44.9% of PC patients and 31.6% of controls (P < 0.008). The mean ages at rst and last SWA episode were 13.5 years (standard deviation [SD] 4.4 years) and 17.1 years (SD 5.3 years), respectively. Subjects who reported SWA also reported more venereal diseases (P < 0.001) and sex with prostitutes (P < 0.001), and were more likely to have had more than 10 lifetime sexual partners (P < 0.001) than those who did not report SWA. SWA with a group of men was reported by 29.8% of subjects and SWA alone was reported by 70.2%. Several animals were used by 62% of subjects, and 38% always used the same animal. The frequency of SWA included single (14%), weekly or more (39.5%), and monthly episodes (15%). Univariate analysis identied phimosis, penile premalignancies, smoking, nonwhite race, sex with prostitutes, and SWA as PC risk factors. Phimosis, premalignant lesions, smoking, and SWA remained as risk factors in multivariate analysis. However, SWA did not impact the clinicopathological outcomes of PC. Conclusion. SWA is a risk factor for PC and may be associated with venereal diseases. New studies are required in other populations to test other possible nosological links with SWA. Zequi SC, Guimares GC, da Fonseca FP, Ferreira U, de Matheus WE, Reis LO, Aita GA, Glina S, Fanni VSS, Perez MDC, Guidoni LRM, Ortiz V, Nogueira L, Rocha LCA, Cuck G, da Costa WH, Moniz RR, Dantas Jr. JH, Soares FA, and Lopes A. Sex with animals (SWA): Behavioral characteristics and possible association with penile cancer. A multicenter study. J Sex Med **;**:****. Key Words. Sex with Animals; Bestiality; Penile Cancer; Zoophilia; Risk Factor; Sexually Transmitted Diseases; HPV

2011 International Society for Sexual Medicine

J Sex Med **;**:****

2
Introduction

Zequi et al. The selected variables were race, age at enrollment, age of rst sexual relationship, history of STD (urethritis, gonorrhea, syphilis, condyloma acuminata, HIV infection), penile premalignant lesions (Queyrats erythroplasia, Bowens disease, lichen sclerosis, balanitis xerotica obliterans, chronic balanitis), phimosis and circumcision, age at circumcision, number of lifetime sexual partners, smoking habits (past or current), history of sex with prostitutes, and SWA. The SWA questions addressed age at rst and last SWA episodes, the frequency of SWA (in days, weeks, months), and the duration of SWA practice in complete years (computed by subtracting the age at the rst SWA episode from the age at the last SWA episode, but only if SWA duration was more than 1 year). We investigated the animal species involved and whether SWA was performed individually or in a group of men, and whether SWA always occurred with the same animal or with several animals. Clinicopathological data for premalignant lesions and PC (histological type, grade, 2002 TNM/UICC [5] (International Union Against Cancer) staging, and therapeutic modality) were obtained from medical records. A central ofce managed the data bank and statistical analyses using Statistical Package for the Social Sciences version 15 (SPSS Inc., Chicago, IL, USA).

enile cancer (PC) is rare in the developed world but frequent in poor regions [1]. Risk factors for PC include unfavorable hygiene, poverty, chronic balanopreputial irritation, premalignant penile lesions, and smoking [2]. Human papillomavirus (HPV) infection is associated with approximately half of PC cases, but its role in PC carcinogenesis has not been clearly established [3]. The role of promiscuity and other sexually transmitted diseases (STDs) in PC is also not completely understood [4]. The present case-control study investigated whether a personal history of sex with animals (SWA), which is a common male sexual practice in rural areas with high PC prevalence, plays a role in PC. We also describe clinical and demographic characteristics of this sexual behavior.

Materials and Methods

Study Design and Subjects Data were collected at 16 tertiary urology or oncology centers in 12 Brazilian cities (Table 1). The subjects included new PC cases and patients previously treated for PC, all of whom were enrolled by mail or by phone. The control group was composed of healthy males aged 18 to 80 years seeking medical attention for benign uropathies, check-up or for cancer prevention. We ascertained that control subjects lived in rural zones during childhood and adolescence and were exposed to animalcontact hazards. Individuals who grew up in an urban environment were excluded. A questionnaire about personal and sexual habits was completed by all subjects via an in-person semi-structured interview with their physicians. This study was approved by our institutional review boards. All subjects provided written informed consent.
Table 1

Statistical Analysis Questionnaire responses from a total of 492 subjects, 118 PC patients and 374 controls (3.16 controls per case), were compared using logistic regression analysis to calculate exposure odds ratios (OR) and 95% condence intervals (CIs) for both groups. The modeling results reect adjusted incidence rate ratios. Proportions were determined using the c2 test or Fishers exact test. Twosided P values <0.05 and 95% CI were considered indicators of signicance. Differences in age were

The rates of sex with animals (SWA) in Brazilian states, cities, and geographical regions
N 287 29 53 14 28 15 20 46 492 Geographic region Southeast Southeast Northeast Northeast Northeast Northeast North South Reporting SWA (%) 94 11 34 8 8 4 6 6 171 (32.8) (37.9) (64.2) (57.1) (28.6) (26.7) (30) (13) (34.8) No SWA (%) 193 18 19 6 20 11 14 40 321 (67.2) (62.1) (35.8) (42.9) (71.4) (73.3) (70) (87) (65.2)

States (cities) So Paulo* (So Paulo, Campinas, Barretos, Itapevi, Carapicuba) Minas Gerais (Belo Horizonte) Piau (Teresina) Maranho (So Lus) Rio Grande do Norte (Natal) Paraba (Joo Pessoa) Acre (Rio Branco) Paran (Curitiba) Total

*Nine hospitals participated from cities in So Paulo state. The rates of SWA were 45%, 33.2%, 20%, and 13% in the northeast, southeast, north, and south, respectively.

J Sex Med **;**:****

Sex with Animals (SWA) and Penile Cancer tested using Students t-test. All signicant explanatory variables in the univariate analysis were entered simultaneously into a logistic regression model. We arrived at a multivariate model using backward elimination to remove the least signicant variables one-by-one until all remaining variables in the model were signicant (P < 0.05 in test for homogeneity). Subsequently, excluded explanatory variables were given another chance to enter the nal model via forward inclusion, but none of the variables previously excluded achieved statistical signicance.
Results

3 erythroplasia, and 0.8% Bowens disease. In the control group, the rates of premalignancies were 4.7% (P < 0.001):1.4% balanitis xerotica obliterans, 2.7% chronic balanitis, 0.3% Bowens disease, and 0.3% lichen sclerosis. A total of 171 individuals (34.8%) reported SWA (Table 1), which was more common among PC patients (44.9%) than controls (31.6%; P = 0.008; Table 2), and among individuals with a history of STDs than those without STDs (56.7% vs. 43.3%; P < 0.001). Subjects who reported SWA also reported more sex with prostitutes (79.5% vs. 59.2%; P < 0.001) and were more likely to have had >10 lifetime sexual partners (64.3% vs. 44.8%; P < 0.001) compared to those who did not report SWA. Penile premalignant lesions occurred in 14.9% of individuals with a history of SWA and in 9% of those without a history of SWA (P = 0.088). Smoking rates among individuals reporting SWA were 56.7% vs. 48.6% for those who did not report SWA (P = 0.086). The mean ages at rst and last SWA episode were 13.5 years (standard deviation [SD] 4.4 years) and 17.1 years (SD 5.3 years), respectively. The mean ages at sexual debut with humans were 16.3 years (SD 7.3 years) and 16.7 years (SD 3.6 years) for subjects who did and did not report SWA, respectively. Independent of SWA status, age at rst intercourse with humans was similar between

The majority of subjects (80.1%) were uncircumcised; 13.4% were circumcised as adults, 3.7% in adolescence, and 2.8% in infancy. The PC and control groups were homogeneous according to age (Table 2). The PC group included more nonwhites (51.8% vs. 36.6%; P = 0.006) and higher rates of smoking (70.3% vs. 45.7%; P < 0.001), phimosis (67.8% vs. 14.4%; P < 0.001), sex with prostitutes (73.7% vs. 63.9%; P = 0.049), premalignant lesions, and SWA compared to the control group (Table 2). In the PC group, the rates of premalignant lesions were 30.3%: 16% balanitis xerotica obliterans, 12.7% chronic balanitis, 0.8% Queyrats
Table 2
Variable Age, years

Univariate analysis of penile cancer (PC) risks


Category Mean 57.57 (SD 14.49) Median: 59 Min: 18 Max: 90 White Black Mulato Asiatic Yes No Yes No Yes No Yes No Yes No 10 >10 Yes No 295 64 122 11 227 265 53 439 253 239 134 358 326 166 237 255 171 321 N PC cases (%) Mean 58.72 (SD 13.00) Median: 58.0 Min: 25 Max: 85 58 23 34 03 (19.7) (35.9) (27.9) (27.3) Controls (%) Mean 57.20 (SD 14.93) Median: 59 Min: 18 Max: 90 237 41 88 08 (80.3) (64.1) (72.1) (72.7) P value* 0.2972

Race

0.036

History of sexually transmitted disease Penile premalignant lesions Smoking Phimosis Sex with prostitutes Number of sexual partners Sex with animals
*c2 test. Students t-test for age.

62 (27.3) 56 (21.1) 36 (67.9) 82 (18.7) 83 (32.7) 35 (14.7) 80 (59.7) 38 (10.6) 87 (27.3) 31 (18.7) 50 (21.1) 68 (26.7) 53 (31.0) 65 (20.2)

165 (72.7) 209 (78.9) 17 (32.1) 357 (81.3) 171 (67.3) 203 (85.3) 54 (40.3) 320 (89.4) 239 (72.7) 135 (81.3) 187 (78.9) 187 (73.3) 118 (69.0) 256 (79.8)

0.068 <0.001 <0.001 <0.001 0.033 0.090 0.008

J Sex Med **;**:****

4 PC patients (17.0 years; SD 8.4 years) and controls (16.5 years; SD 3.7 years). SWA periodicity varied. A single SWA lifetime episode was reported by 14% of SWA-reporting subjects. SWA episodes were reported at frequencies of twice per month (17%), monthly (15.2%), weekly (10.5%), three times per week (10%), twice per week (9.4%), daily (4.1%), and every other day (5.3%). Bimonthly, semiannual, and quarterly SWA was reported by 3.5%, 2.9%, and 2.3%, respectively. In two cases (1.2%), the frequency was not reported. The duration of SWA behavior was less than 1 year in 34 individuals (19.9%). In the 137 subjects (80.1%), it ranged from 1 to 26 years (mean 4.47 years, SD 3.8 years; median 3.0 years). Durations of 1 to 5 years were reported by 101 individuals (59%), and 36 subjects (21.1%) described SWA behavior as persisting for more than 5 years. High SWA periodicity (daily, alternate days, three or more times per week, twice per week, biweekly, and monthly) and long-term SWA were associated; 87.2% of individuals reporting >3 years of SWA also reported high-periodicity SWA, compared with 55.3% of those reporting <3 years of SWA (P < 0.001). SWA with a group of men was reported by 29.8% of SWA-reporting study participants, with similar rates reported by PC patients (34%) and controls (28%; P = 0.396). SWA was practiced with the same animal by 38.0% of SWA practitioners, with similar rates reported by PC patients and controls (34% vs. 39.8%, respectively; P = 0.638). The number of animals involved per individual ranged from 1 to 7. The animal types most often cited were mares (N = 80), followed by donkeys (N = 73), mules (N = 57), goats (N = 54), chickens (N = 27), calves (N = 18), cows (N = 13), dogs (N = 10), sheep (N = 10), pigs (N = 6), and other species (N = 3). Chickens were more frequently involved in the south and southeast of the country, with only three reports in the northeast, where donkeys dominated the reports. Higher SWA rates were found in the northeast (45%), with the highest rates in Piau and Maranho (Table 1). Among the 171 men who reported SWA, 50 (29.2%) had PC. In these men, no association was detected between PC and the number of animals (always the same animal vs. several animals, P = 0.417), species (P = 0.679), or the number of people involved (SWA alone or in a group, P = 0.290). Individualized SWA periodicities were not associated with PC (P = 0.19). In addition,
J Sex Med **;**:****

Zequi et al. high or low SWA periodicity was not associated with PC. High SWA periodicity was reported by 78% of the PC patients and 68.1% of the controls (P = 0.263). Long-term SWA (>3 years) was reported by 64% of the PC patients and 46.6% of the controls (P = 0.044). The predominant PC histology was squamous cell carcinoma (50.8% welldifferentiated, 29.6% moderately differentiated, and 11% undifferentiated). Carcinoma in situ, verrucous carcinoma, sarcoma, and other forms occurred in 2.5%, 3.4%, 0.8%, and 1.9% of PC cases, respectively. Low grade (I/II), high grade (III/IV), and unspecied ignored grade were indicated in 76.7%, 13.8%, and 9.5% of cases, respectively. Supercial tumors occurred in 55.1% of PC cases (pTa or pTis in 6.8% and pT1 in 48.3%) and invasive tumors ( pT2) in 44.9% of PC cases. Negative inguinal lymph nodes occurred in 72.9% of cases. Three patients (2.5%) had distant metastases. Primary tumor treatments included partial penile amputation (72%), total penile amputation (10%), tumor exeresis or postectomy (8.5%), and other treatments (9.5%). Eighty-nine patients (75.4%) were alive without disease, and 29 (25.6%) were alive with cancer at the time of the study. SWA behavior was not signicantly associated with histological type (P = 0.201), grade (P = 0.310), treatment (P = 0.346), pT stage (P = 0.857), pN stage (P = 0.177), pM stage (P = 0.270), or clinical status (P = 0.396). Univariate analysis (Table 2) revealed the following risk factors for PC: phimosis (P < 0.001), premalignant lesions (P < 0.001), smoking (P < 0.001), SWA (P = 0.008), race (white vs. nonwhite; P = 0.007), and sex with prostitutes (P = 0.033). In the multivariate analysis (Table 3), phimosis (OR 10.41, 95% CI 6.1217.67; P < 0.001), premalignant lesions (OR 3.90, 95% CI 1.888.09; P < 0.001), smoking (OR 2.71, 95% CI 1.594.62; P < 0.001), and SWA (OR 2.07, 95% CI 1.213.52; P = 0.007) were risk factors for PC.
Discussion

The practice of having SWA has been present since ancient times [6]. SWA is underreported in the medical literature, but has been transmitted through oral traditions, it is present in artistic representations, and was prohibited by the Bible (Exod 22:28; Lev 20:16) [68]. This behavior may be interpreted as curiosity or as experiences preceding male sexual maturity [9]. Kinsey reported that 8% of Americans had some SWA experience,

Sex with Animals (SWA) and Penile Cancer


Table 3
Variable Phimosis Penile premalignant lesions Smoking Sex with animals Race (nonwhite vs. white) Sex with prostitutes

Multivariate analysis of penile cancer risk factors


Odds ratio 10.41 3.90 2.71 2.07 0.63 0.83 95% condence interval 6.1217.67 1.888.09 1.594.62 1.213.52 0.3751.05 0.461.47 P value <0.001 <0.001 <0.001 0.007 0.078 0.514

and afrmed that SWA is common among teen farmers of low intelligence [10]. Others consider SWA as something other than a simple substitutive phenomenon, such as a psychopathic manifestation of neurosis or psychosis [8]. In small samples of psychiatric inpatients, medical inpatients, and psychiatric staff, the prevalence of bestiality (sexual contact or only fantasy) was 55%, 10%, and 15%, respectively, but sexual contact was veried only among male psychiatric inpatients. All groups had similar SWA fantasy rates [11]. In this population, the majority of subjects reporting SWA stopped the practice around the period that they began sexual contact with humans; thus, in the context of the present study, SWA must be distinguished from established bestiality or zoophilia, paraphilias represented by continuous or obsessive desires for SWA instead of sex with human partners [5,7,9]. An online questionnaire with 114 self-dened zoophiles in developed countries revealed that 36% lived in large cities and 83% were either college graduates or had completed some college. Fortyve percent of the respondents worked in informatics or technology, some of them with high income [6]. However, third-world PC patients exhibit the opposite socioeconomic and cultural characteristics. The motivation for this study came from the observation that the majority of PC patients originate from poor rural zones, a typical environment for SWA occurrence. This rural determinant was used as a main condition in recruiting the control population. We excluded men that grew up in an urban environment, because PC prevalence is anecdotal in these regions, suggesting that this population is at little risk of developing this malignancy. Furthermore, the opportunities for an urban teenager to be in contact with animals in a situation allowing sexual activity are restricted. In contrast, boys in rural areas live daily with animals, with several opportunities of having sexual contact with them. Thus, by choosing individuals from

rural areas, we ensured that both cases and controls were under the same odds of intimate contact with animals and faced with the same decisions regarding consummation. In addition, the homogeneity of age between PC patients and control subjects was fundamental. In the last few decades, sexual freedom has favored earlier sexual contacts, probably reducing sexual contact with animals. An age bias would thus have introduced additional biases into the investigation. Our study relied on in-person semi-structured interviews because many of the study participants are illiterate or partially literate, which would compromise comprehension of the questionnaire. Although other biases may be introduced by this format, such as inhibition or lying, the anonymity of web-based or written questionnaires does not imply total veracity. SWA emerged as a risk factor for PC in the multivariate analysis (Table 3). We hypothesize that SWA promotes contact of penile tissues with foreign genital mucosa, resulting in microtrauma and exposure to the animals anogenital secretions, which may be antigenic or carcinogenic for humans. This situation would favor chronic irritation processes and subsequent dysplasia. Penile injuries, tears, abrasions, or balanitis are known to increase PC risk [2,4,1216]. Additionally, 51.4% of the study population smoked, 14% of SWA participants had premalignancies, and the majority of subjects were uncircumcised or circumcised later in life. This situation is associated with other environmental PC risk factors, such as poor hygienic conditions, poverty, and HPV infection [2,4,1218], which may potentiate conditions for PC development. The link between SWA and PC and its association with STDs may reect the SWA practitioners lifestyle. The subjects that reported SWA had more sex with prostitutes, more sexual partners, and more STDs than subjects who did not report SWA; moreover, 29.8% of them practiced SWA with a group of men, 64.9% had sex with multiple animals.
J Sex Med **;**:****

6 We identied a high rate of uncircumcised men with PC, although the role of unknown infectious agents (virus, bacteria, or other microorganisms) [9,19] in interspecies sexual contact can not be completely discarded. Some neoplasias are associated with infections, such as links between uterine cervical cancer or anogenital carcinomas and HPV infections or gastric carcinoma and presence of Helicobacter pylori [19,20]. Recent reports have also described a possible pathogenic role of XMRV retrovirus [21,22] in prostate cancer, another genital organ neoplasia, as well as a role of prions in tumorigenesis [23]. The penis may also be susceptible to infections in addition to HPV. Prolonged and continuous SWA exposure in our study population (60% practiced SWA over 15 years and 20% for more than 5 years, many of them several times a month or weekly) would increase the opportunities for penile microtrauma and may facilitate exposure to infectious agents present in the external environment. Speculation exists regarding cancer status as an infectious disease in humans [24,25], as studies have suggested that tumor cells can be transmitted from one mammal host to another within the same species [26,27]. PC is frequent in equines [28], but transmission of malignancies between animals and humans has not been reported. Virology does not consider possible viral movement from animals to humans except in cases of zoonosis, such as rabies or pandemic forms of bird or swine u. However, the hypothesis that the HIV epidemic resulted from simianhuman virus transmission has not been fully explored [29]. Fewer southern and northern Brazilian institutions were evaluated because PC is rare in the south [17] and the north has low population density. SWA was more frequent in the poorest Brazilian region, the northeast, and the rates were lowest in the southern region, which is developed and urbanized (Table 1). The kind of animals involved in SWA varied according to the domestic species that are typical of each region. The use of the same animal by 34.5% of SWA participants may be due to poverty, as the individual only has one animal, or some affective relationship with the animal. This study was hindered by a few limitations. We did not investigate the sexual orientation of the SWA practitioners regarding animals or human partners. For example, how many of these men were engaging in sex with men? In what types of sexual activity did the SWA-positive men and
J Sex Med **;**:****

Zequi et al. the animals engage? We assumed that our study subjects penetrated the animal vaginally or anally; we did not investigate other possibilities. We did not evaluate condom use, but we think that during the period in which these patients participated in SWA (before the AIDS era), condom use was not as widespread as it is nowadays. Specic pathological features or clinical outcomes of PC were not detected in the sample, probably due to the sample size and the nature of the retrospective data from several institutions with different treatment protocols. A central pathological review in association with a molecular investigation of HPV in a large PC cohort is underway. Our ndings were based on self-reported history of SWA. Since self-report surveys may be questionable and are subject to recall bias, the ideal would be to design observational prospective cohort studies. However, we reiterate the several technical and ethical difculties involved in a study of this nature on this issue, beyond the assumption that the practice of SWA could put patients under risk of morbid conditions. Although this study reects the sexual practices of a population that occurred decades ago (especially during the adolescence of the subjects), SWA is a worldwide practice. There are several zoophilic associations or clubs in developed countries [7] and many zoo web sites and virtual communities on the Internet [6] that are frequently associated with pornographic content, and may constitute a global health concern. Studies must be performed in several countries and civilizations with different incidences of PC and STDs, as well as on rural, indigenous and urban communities, on females, and in urological cancer facilities. Considering future prevention strategies, investigations of SWA in Africa would be interesting, as studies have already demonstrated a protective role of male circumcision against several STDs [3032]. Novel possible associations between SWA and urological diseases might be tested, including non-traumatic urethral stenosis, idiopathic infertility, and chronic prostatitis. Health campaigns should be discussed to promote the refutation of SWA in target populations. In extreme refractory cases, condom use or other barrier methods should be suggested to minimize the risks of this sexual option, although this is ethically debatable. SWA merits serious scientic attention due to its high prevalence and associated risks for PC and perhaps STDs. Initiatives to eradicate SWA should be considered.

Sex with Animals (SWA) and Penile Cancer


Acknowledgments

7
Fonseca; Ademar Lopes; Fernando Augusto Soares; Sidney Glina; Wagner Eduardo de Matheus; Gustavo Cuck; Walter Henriques da Costa (b) Revising It for Intellectual Content Stnio de Cssio Zequi; Ubirajara Ferreira; Giuliano Amorim Aita; Victor Silvestre Soares Fanni; Marjo Denisson Cardenuto Perez; Luiz Renato Montez Guidoni; Valdemar Ortiz; Lucas Nogueira; Luis Carlos de Almeida Rocha; Ravendra Ryan Moniz; Jos Hiplito Dantas Jr.

The authors thank the Penile Cancer Study Group (PCSG) members: Sandro Nassar Cardoso, MD (Urology Division, Hospital Ipiranga, So Paulo, SP, Brazil), Roni de Carvalho Fernandes, MD (Urology Division of Surgical Department FCMSCSP, Faculdade de Cincias Mdicas da Santa Casa de So Paulo, SP, Brazil), Jose Vassalo, PhD (Surgical and Investigative Pathology Department, Hospital A C Camargo, So Paulo, SP, Brazil), Fernando Assis Melo, MD (Urology Service, FUNDACRE, Fundao Hospitalar do Acre, Rio Branco, AC, Brazil), Jos Ribamar Rodrigues Calixto, MD (Urology Departament, Hospital Universitrio da Universidade Federal do Maranho, MA, Brazil), Marcus Mattos, MD (Urology Service, Hospital Geral de Itapevi, SP, Brazil), Daniel Damio Gomes Seabra, PhD (Urology Department, Hospital do Cncer de Barretos, Fundao Pio XII, Barretos, SP, Brazil), Cristiano Utida, MD (Urology Department, UNIFESP, Universidade Federal de So Paulo, So Paulo, SP, Brazil), Fbio Martinez de Melo, MD (Urology Division, Hospital Napoleo Laureano, Joo Pessoa, PB, Brazil), Djalma de Carvalho Moreira Filho, PhD (Public Health and Preventive Medicine Department of UNICAMP, Universidade Estadual de Campinas, Brazil). Corresponding Author: Stnio de Cssio Zequi, PhD, Urology Division of Pelvic Surgery Department, Hospital A C Camargo, Rua Professor Antnio Prudente, 211, So Paulo 01509 010, Brazil. Tel: 5511 2189 5000; Fax: 5511 38849103; E-mail: steniozequi@uol.com.br, steniozequi@gmail.com Conict of Interest: None.
Statement of Authorship

Category 3
(a) Final Approval of the Completed Article Stnio de Cssio Zequi; Gustavo Cardoso Guimares; Francisco Paulo da Fonseca; Ubirajara Ferreira; Wagner Eduardo de Matheus; Leonardo Oliveira Reis; Giuliano Amorim Aita; Sidney Glina; Victor Silvestre Soares Fanni; Marjo Denisson Cardenuto Perez; Luiz Renato Montez Guidoni; Valdemar Ortiz; Lucas Nogueira; Luis Carlos de Almeida Rocha; Gustavo Cuck; Ravendra Ryan Moniz; Jos Hiplito Dantas Jr.; Fernando Augusto Soares; Ademar Lopes
References 1 Curado MP, Edwards B, Shin HR, Storm H, Ferlay J, Heanue M, Boyle P. Cancer incidence in ve continents. Vol. IX [IARC Scientic Publications, 160]. Lyon: IARC; 2007. 2 Pow-Sang MR, Ferreira U, Pow-Sang JM, Nardi AC, Destefano V. Epidemiology and natural history of penile cancer. Urology 2010;76(1 suppl):S26. 3 Miralles-Guri C, Bruni L, Cubilla AL, Castellsagu X, Bosch FX, de Sanjos S. Human papillomavirus prevalence and type distribution in penile carcinoma. J Clin Pathol 2009;62:8708. 4 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;85:1924. 5 Sobin LH, Wittekind C, eds. TNM classication of malignant tumors. 6th edition. New York, NY: Wiley & Sons; 2002. 6 Williams CJ, Weinberg MS. Zoophilia in men: A study of sexual interest in animals. Arch Sex Behav 2003;32:52335. 7 Miletski H. Understanding bestiality and zoophilia. Bethesda, MD: East-West Publishing LLC; 2002: 273 pp. 8 Shenken LI. Some clinical and psychopathological aspects of bestiality. J Nerv Ment Dis 1964;139:13742. 9 Karpman B. The sexual offender and his offenses: Etiology, pathology, psychodynamics, and treatment. New York: Julian Press; 1954. 10 Kinsey AC, Pomeroy WB, Martin CE. Sexual behavior in the human male. Philadelphia: W.B. Saunders; 1948. 11 Alvarez WA, Freinhar JP. A prevalence study of bestiality (zoophilia) in psychiatric in-patients, medical in-patients and psychiatric staff. Int J Psychosom 1991;38:457. 12 Tseng HF, Morgenstern H, Mack T, Peters RK. Risk factors for penile cancer: Results of a population-based case-control study in Los Angeles County (United States). Cancer Causes Control 2001;12:26777. 13 Daling JR, Madeleine MM, Johnson LG, Schwartz SM, Shera KA, Wurscher MA, Carter JJ, Porter PL, Galloway DA, McDougall JK, Krieger JN. Penile cancer: Importance of circumcision, human papillomavirus and smoking in in situ and invasive disease. Int J Cancer 2005;116:60616.

Category 1
(a) Conception and Design Stnio de Cssio Zequi (b) Acquisition of Data Stnio de Cssio Zequi; Wagner Eduardo de Matheus; Leonardo Oliveira Reis; Giuliano Amorim Aita; Victor Silvestre Soares Fanni; Luiz Renato Montez Guidoni; Lucas Nogueira; Gustavo Cuck; Walter Henriques da Costa; Ravendra Ryan Moniz; Jos Hiplito Dantas Jr. (c) Analysis and Interpretation of Data Stnio de Cssio Zequi; Gustavo Cardoso Guimares; Francisco Paulo da Fonseca; Leonardo Oliveira Reis; Giuliano Amorim Aita; Sidney Glina; Valdemar Ortiz; Luis Carlos de Almeida Rocha; Fernando Augusto Soares; Marjo Denisson Cardenuto Perez; Ademar Lopes

Category 2
(a) Drafting the Article Stnio de Cssio Zequi; Gustavo Cardoso Guimares; Leonardo Oliveira Reis; Francisco Paulo da

J Sex Med **;**:****

8
14 Hellberg D, Valentin J, Eklund T, Nilsson S. Penile cancer: Is there an epidemiological role for smoking and sexual behaviour? Br Med J (Clin Res Ed) 1987;295:13068. 15 Wideroff L, Schotteneld D. Penile cancer. In: Schottenfeld D, Fraumeni JF, eds. Cancer epidemiology and prevention. New York: Oxford University Press; 2006:116672. 16 Edlin RS, Aaronson DS, Wu AK, Blaschko SD, Yang G, Erickson BA, McAninch JW. Squamous cell carcinoma at the site of a Prince Alberts piercing. J Sex Med 2010;7:22803. 17 Favorito LA, Nardi AC, Ronalsa M, Zequi SC, Sampaio FJ, Glina S. Epidemiologic study on penile cancer in Brazil. Int Braz J Urol 2008;34:58791. 18 Crispen PL, Mydlo JH. Penile intraepithelial neoplasia and other premalignant lesions of the penis. Urol Clin North Am 2010;37:33542. 19 Velzquez E, Peix A, Gmez-Alonso A. Microorganisms and cancer: Scientic evidence and new hypotheses. Cir Esp 2011;89:13644. 20 Dalton-Grifn L, Kellam P. Infectious causes of cancer and their detection. J Biol 2009;8:67. 21 Urisman A, Molinaro RJ, Fischer N, Plummer SJ, Casey G, Klein EA, Malathi K, Magi-Galluzzi C, Tubbs RR, Ganem D, Silverman RH, DeRisi JL. Identication of a novel Gammaretrovirus in prostate tumors of patients homozygous for R462Q RNASEL variant. PLoS Pathog 2006;2:e25. 22 Silverman RH, Nguyen C, Weight CJ, Klein EA. The human retrovirus XMRV in prostate cancer and chronic fatigue syndrome. Nat Rev Urol 2010;7:392402. 23 Mehrpour M, Codogno P. Prion protein: From physiology to cancer biology. Cancer Lett 2010;290:123. 24 Grtner HV, Seidl C, Luckenbach C, Schumm G, Seifried E, Ritter H, Bltmann B. Genetic analysis of a sarcoma accidentally transplanted from a patient to a surgeon. N Engl J Med 1996;335:14946.

Zequi et al.
25 Dingli D, Nowak MA. Cancer biology: Infectious tumour cells. Nature 2006;443:356. 26 Murgia C, Pritchard JK, Kim SY, Fassati A, Weiss RA. Clonal origin and evolution of a transmissible cancer. Cell 2006;126:47787. 27 Rebbeck CA, Thomas R, Breen M, Leroi AM, Burt A. Origins and evolution of a transmissible cancer. Evolution 2009;63:23409. 28 van den Top JG, de Heer N, Klein WR, Ensink JM. Penile and preputial tumours in the horse: A retrospective study of 114 affected horses. Equine Vet J 2008;40:52832. 29 Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Cummins LB, Arthur LO, Peeters M, Shaw GM, Sharp PM, Hahn BH. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 1999;397:43641. 30 Weiss HA, Thomas SL, Munabi SK, Hayes RJ. Male circumcision and risk of syphilis, chancroid, and genital herpes: A systematic review and meta-analysis. Sex Transm Infect 2006;82:1019. 31 Gray RH, Kigozi G, Serwadda D, Makumbi F, Watya S, Nalugoda F, Kiwanuka N, Moulton LH, Chaudhary MA, Chen MZ, Sewankambo NK, Wabwire-Mangen F, Bacon MC, Williams CF, Opendi P, Reynolds SJ, Laeyendecker O, Quinn TC, Wawer MJ. Male circumcision for HIV prevention in men in Rakai, Uganda: A randomised trial. Lancet 2007;369:65766. 32 Tobian AA, Serwadda D, Quinn TC, Kigozi G, Gravitt PE, Laeyendecker O, Charvat B, Ssempijja V, Riedesel M, Oliver AE, Nowak RG, Moulton LH, Chen MZ, Reynolds SJ, Wawer MJ, Gray RH. Male circumcision for the prevention of HSV-2 and HPV infections and syphilis. N Engl J Med 2009;360:1298309.

J Sex Med **;**:****

You might also like