Academic Journal of Suriname 2011, 2, 198-204 Biomedicine Full-length paper

The incidence of malignancies of the male urogenital system in the Republic of Suriname from 1980 through 2004

Dennis R.A. Mans 1, Santosh S. Sardjoe 1, Martinus A. Vrede 2

1Department of Pharmacology, Faculty of Medical Sciences, Anton de Kom University of Suriname, Paramaribo, Suriname; 2Department of Pathology, Faculty of Medical Sciences, Anton de Kom University of Suriname, Paramaribo, Suriname

Abstract

The worldwide occurrence of male urogenital malignancies ( of prostate, penis, and testes, as well as those of kidneys and urinary bladder of men) varies from exceedingly rare to very common. In this study, incidence rates of these in the Republic of Suriname between 1980 and 2004 have been assessed and compared with international data. Patient information was obtained from the Pathologic Anatomy Laboratory, population data from the General Bureau of Statistics. Sex-specific rates were calculated for overall and for all anatomical sites, and stratified according to age groups 0 to 19, 20 to 49, and 50+ years, as well as the largest ethnic groups, viz. Hindustani, Creole, and Javanese. From these data, average yearly numbers and average rates per 100,000 men per year were calculated and expressed as means ± SDs. There were nearly 900 male urogenital malignancies in the period covered by this study, which corresponded to an overall rate of approximately 17. The most common urogenital by far was prostatic cancer, occurring in more than three- quarters of cases and at a rate of about 13. Kidney, urinary bladder, penile, and were seen at rates lower than 2. The vast majority of patients, particularly those suffering from prostatic cancer, was 50 years and older and Creole. Notwithstanding, when compared with low- and high-incidence areas throughout the world, Suriname seems to represent a low-risk country for male urogenital malignancies including prostatic cancer. More comprehensive epidemiological studies in the multi-ethnic and multi-cultural society of Suriname may contribute to our understanding of the etiology of cancer.

Key words: male urogenital cancers; Suriname; incidence rates; age group; ethnic background

Introduction higher the grade and the stage of the tumor at presentation, the poorer the prognosis (Hellerstedt and Pienta, 2002; Micali et al., 2006; Barocas and Clark, Malignancies of the male urogenital system 2008; Feldman et al., 2008; Djouadou et al., 2010; Sun originate from prostate, penis, and testes, as well as et al., 2010). The main exception is testicular cancer, the kidneys and urinary bladder of men. These neoplasms treatment of which is regarded as one of the success are usually treated with surgery, , stories of modern medicine, producing sustained and/or (Micali et al., 2006; Barocas and responses in more than 90% of cases regardless of stage Clark, 2008; Feldman et al., 2008; Djouadou et al., 2010; (Feldman et al., 2008). Sun et al., 2010), and in the case of prostatic cancer, also Although the specific causes of male urogenital hormonal therapy in the form of androgen ablation malignancies remain unknown, a number of risk factors (Hellerstedt and Pienta, 2002). The efficacy of these has been identified. For prostatic cancer, these include, therapeutic modalities depends primarily on the stage of among others, an average age of 70 years (Hankey et al., the disease at the time of diagnosis. Generally speaking, 1999); the presence of first-degree family members with early diagnosis results in a better prognosis, but the

Correspondence to: Dennis R.A. Mans, PhD, Department of Pharmacology, Faculty of Medical Sciences, Anton de Kom University. Kernkampweg 5-7, Paramaribo, Suriname. Tel/Fax: 597 441071. E-mail: [email protected]

Available on-line October 25, 2011

Acad J Sur 2011 (2) 198-204 Incidence of male urogenital cancers in Suriname 199

this disease (Zeegers et al., 2003); being from African We previously reported on various aspects of descent (Brawley et al., 1998; American Cancer Society, the epidemiology of cancer in Suriname (Mans et al., 2005); and the consumption of diets high in fat but low 2003, 2007, 2008, 2010), and more recently, on the in fresh vegetables and fruits (Ma and Chapman, 2009). incidence of genitourinary malignancies in Surinamese In addition to advanced age, the risk factors for penile women (Mans et al., 2011). So far, however, no cancer include poor personal hygiene, phimosis, the comprehensive data are available on the occurrence of absence of circumcision, and infection with oncogenic urogenital malignancies in Surinamese men. For this human viruses (Madsen et al., 2008; Pow- reason, we decided to determine incidence rates of this Sang et al., 2010). Testicular cancer, on the other hand, group of neoplasms in the country, overall, as well as occurs commonly at age 20 to 39 years (Hayes-Lattin according to anatomical location, age at the time of and Nichols, 2009), in Caucasians (Shah et al., 2007), diagnosis, and ethnic background. The results have been and in men with cryptorchidism (Diekman and discussed against the background of data from low- and Pichlmeier, 2004). Renal neoplasms have been related to high-incidence countries throughout the world. end-stage renal disease (Stewart et al., 2009), hereditary predispositions such as von Hippel-Lindau syndrome Patients and methods and tuberous sclerosis (Clague et al., 2009), and environmental exposures such as analgesic abuse (Gago- Dominguez et al., 1999) and tobacco smoking (Tsivian Study population and sources of data et al., 2011). Urinary has mainly been In this survey, the incidence of malignancies of associated with tobacco smoking (Strope and Montie, the male urogenital system in Suriname for the period 2008), as well as environmental exposures in many between 1980 and 2004 has been determined. Benign Western countries (Ploeg et al., 2009), and chronic neoplasms, in situ , and non-malignant skin infection with Schistosoma hematobium in certain cancers have been excluded from the study. developing countries (Parkin, 2006). Numbers of diagnoses have been obtained from Prostatic cancer is the second most frequently the records of the Pathologic Anatomical Laboratory of diagnosed cancer and the sixth leading cause of cancer the Academic Hospital Paramaribo. This institution is death in males worldwide (Jemal et al., 2011), and the the reference center for histopathological diagnosis of second most important cause of cancer mortality in cancer and for registration of all histopathologically males in the United States of America (USA) after lung diagnosed cancer cases in Suriname. The records also cancer (Jemal et al., 2010). In 2008, there were 903,500 provided information about the anatomical location of new patients with prostatic cancer throughout the world, the malignancies, the age of the patients at the moment representing 14% of overall new cancer cases, 258,400 of diagnosis, their gender, and their ethnic background. of whom died from their disease (Jemal et al., 2011). Estimations of the mid-year population size of The number of affected individuals in industrialized Suriname in the period covered by this study were countries exceeds that in Third World countries by more provided by the Section Population Statistics of the than five-fold (Jemal et al., 2011). This difference is General Bureau for Statistics, Ministry of Planning and largely attributable to the higher prevalence of risk Developmental Cooperation (General Bureau for factors in the former areas such as a longer life Statistics, 2003). expectancy and certain dietary patterns (Baade et al., 2009), as well as the higher detection rate because of Data processing better access to screening programs (Quinn and Babb, For each year in the period 1980 through 2004, 2002). Tumors of the kidney, urinary bladder, penis, and the total number of male urogenital cancers overall; the testis are much more uncommon, constituting about 2.5, total number of cancers per anatomical location 4.5, 1.0, and 0.8%, respectively, of all cancers in males (kidneys, urinary bladder, prostate, testis, and penis); the worldwide (Janout and Janoutová, 2004; Jemal et al., total number of cases in the age groups 0 to 19 years, 20 2011; Ploeg et al., 2009). However, whereas penile to 49 years, and 50 years and older; as well as the total cancer accounts for only 0.2% of neoplasms in North number of cases in the three largest ethnic groups American and European men, it comprises 10% of male (Hindustani, Creole, and Javanese) have been cancers in some parts of Africa and South America determined. For each of these subgroups, mean yearly (Antunes et al., 2007). numbers were calculated by dividing the sums by 25. The Republic of Suriname is located in the For each sub-stratum, yearly sex-specific rates north-eastern section of South America and has as its were obtained by dividing the number of cases in a capital city Paramaribo. The population of particular subgroup in a particular year by the size of the approximately 525,000 consists of Amerindians, the mid-year male population in that year, and were original inhabitants; Maroons, originating from African expressed per 100,000 men per year. Mean sex-specific slaves who arrived between the 16 th and the 19 th century; rates for each sub-stratum were obtained by adding up Creoles, a generic term referring to individuals with one the rates from 1980 to 2004 and dividing the sums by 25. or more African ancestors; the descendants from contract workers attracted from China, India, and Java Statistics (Indonesia) between the second half of the 19 th and the Data presented are means ± SDs, and have been first half of the 20 th century; as well as immigrants from evaluated for statistically significant differences on the several European and Middle East countries (Helman, basis of p values < 0.05 according to ANOVA. 1977; General Bureau for Statistics, 2003). Acad J Sur 2011 (2) 198-204 200 Mans et al.

Results 3, and 3 and 1 case(s), respectively, per year (Table 2). These values corresponded to sex-specific rates of about 1 to 3 case(s) per 100,000 men per 2 years, and did not Generalities differ significantly from each other (Table 2). In the period between 1980 and 2004, 899 overall male urogenital malignancies were diagnosed in Suriname (Table 1). This corresponded to about 36 new Table 2. Total and average number of diagnoses (± SDs) per year, as well as average sex-specific rates (± SDs) cases per year or 1 new case every 10 days, and a yearly per year of individual male urogenital malignancies in sex-specific rate of roughly 17 new cases per 100,000 Surinamese men in the period between 1980 and 2004. men (Table 1). This group of cancers had a clear Sex-specific rates are per 100,000 men per year. predilection for older men (Table 1). There were less Discrepancies between the number of overall cases than 2 cases per year in males younger than 50 years mentioned in Table 1 and the total number of cases given (Table 1), but almost 34 per year in men of 50 years and below were due to the absence of information about the older (Table 1). Furthermore, these malignancies anatomical location of the tumor in some cases. manifested preferentially in Creoles rather than in males from other ethnic backgrounds (Table 1). Almost two- thirds of overall cases (562 of 899) were diagnosed in Total Average Average Creoles, and only 7 to 10% in Hindustanis and Javanese number yearly sex- (Table 1), with no statistically significant differences of cases number of specific between the latter two groups. cases rate

Table 1. Total and average number of diagnoses (± SDs) Prostate 692 27.7 ± 19.9 13.0 ± 8.5 1 1 per year, as well as average sex-specific rates (± SDs) Urinary bladder 85 3.3 ± 2.0 1.6 ± 1.0 1 1 per year of male urogenital malignancies overall; in age Penis 67 2.8 ± 1.3 1.4 ± 0.7 1 1 groups 0 to 19 years, 20 to 49 years, and 50 years and Kidneys 28 1.2 ± 1.2 0.6 ± 0.6 1 1 older; and in Hindustanis, Creoles, and Javanese in Testes 22 0.8 ± 0.6 0.4 ± 0.3 Suriname in the period between 1980 and 2004. Sex- specific rates are per 100,000 men per year. Total 894 - -

Total Average Average 1Significantly different from ‘Prostate’ (P < 0.001) number yearly number sex- of cases of cases specific rate Distribution according to age group The distribution of male urogenital Total 899 36.0 ± 20.2 17.1 ± 8.3 malignancies according to age group is presented in

1 1 Table 3. As found for cancer overall, the vast majority of 0 - 19 years 7 0.3 ± 0.5 0.1 ± 0.3 cancer cases was seen in individuals of 50 years and 20 - 49 years 26 1.0 ± 1.5 1 0.5 ± 0.7 1 50+ years 846 33.8 ± 15.3 1 16.2 ± 6.1 older, while there were no or very few cases in the Unknown 20 - - groups of 0 to 19 and 20 to 49 years. This trend was most apparent for prostatic cancer: almost all diagnoses Hindustanis 95 4.0 ± 2.4 2 1.8 ± 1.1 2 (689 of the 692) were in men of 50 years and older. Creoles 562 22.5 ± 11.9 10.7 ± 4.8 Cancers of the urinary bladder and penis were less Javanese 60 2.9 ± 2.1 2 2.9 ± 1.0 2 common than prostatic cancer, but occurred also at a

Others 182 - - significantly higher rate in males of 50 years and older when compared to younger men. The three age groups did not differ statistically significantly from each other 1Significantly different from ‘50+ years’ (P < 0.001); 2significantly different from ‘Creoles’ (P < P < 0.001). with respect to the average frequencies of kidney and testicular cancer. However, these neoplasms seemed to manifest at relatively high proportions (approximately Distribution according to anatomical location 30%) in individuals younger than 50 years. As shown in Table 2, prostatic cancer represented by far the most common male urogenital Distribution according to ethnic background malignancy in Suriname, comprising roughly 700 of the approximately 900 diagnoses, or more than three Table 4 provides the ethnic distribution of male quarters of overall cases. There were on average 28 new urogenital cancers between 1980 and 2004. Almost 70% cases per year ( i.e. , roughly 1 every 2 weeks), which of the 692 cases of prostatic cancer registered in this corresponded to a sex-specific rate of about 13 new period were encountered in Creoles, and only 5 to 8% in patients per 100,000 men per year (Table 2). Cancers of Javanese and Hindustanis. Sex-specific rates were the kidneys and urinary bladder, as well as those of penis approximately 9, and about 1 per 100.000 men per year and testes comprised together approximately 20% of for Creoles, Hindustanis and Javanese, respectively. male urogenital cancers in the period covered by this Cancers of the urinary bladder and penis were also more study, and occurred at approximate frequencies of 1 and common in Creoles than in Hindustanis and Javanese, with no significant differences between the latter two Acad J Sur 2011 (2) 198-204 Incidence of male urogenital cancers in Suriname 201

groups in average yearly numbers of cases and average Kidney and testicular cancer seemed to be present at yearly sex-specific rates. However, the proportion of comparable frequencies in the three ethnic groups, i.e. , at Javanese men with (5 out of a total of 67) sex-specific rates of 1 to 2 cases per 100,000 men per 10 was markedly lower than that of Hindustani men years. suffering from this disease (14 out of a total of 67).

Table 3. Total and average number of diagnoses (± SDs) per year as well as average sex-specific rates (± SDs) per year of urogenital malignancies in Surinamese men of 0 to 19 years, 20 to 49 years, and 50 years and older in the period between 1980 and 2004. Sex-specific rates are per 100,000 men per year. Discrepancies between the number of overall cases mentioned in Table 1 and the total number of cases given below, were due to the absence of information about the age of the patients in some cases.

0 - 19 years 20 - 49 years 50+ years

Total Average Average Total Average Average Total Average Average number yearly sex- number yearly sex- number yearly sex- of cases number specific of cases number specific of cases number specific of cases rate of cases rate of cases rate

Prostate 0 0.0 ± 0.0 1 0.0 ± 0.0 1 3 0.1 ± 0.3 1 0.1 ± 0.2 1 689 27.6 ± 19.9 13.0 ± 8.2 Urinary bladder 1 0.1 ± 0.2 1 0.0 ± 0.1 1 5 0.1 ± 0.3 1 0.1 ± 0.2 1 79 3.2 ± 2.4 1.5 ± 1.1 Penis 2 0.1 ± 0.3 1 0.0 ± 0.1 1 7 0.4 ± 0.5 1 0.2 ± 0.2 1 58 2.3 ± 1.3 1.2 ± 0.7 Kidneys 2 0.1 ± 0.4 0.0 ± 0.2 6 0.4 ± 0.6 0.1 ± 0.3 20 0.8 ± 0.8 0.4 ± 0.4 Testes 2 0.1 ± 0.3 0.0 ± 0.1 5 0.2 ± 0.4 0.1 ± 0.2 15 0.6 ± 0.6 0.3 ± 0.3

Total 7 - - 26 - - 861 - -

1Significantly different from ‘50+ years’ (P < 0.001).

Table 4. Total and average number of diagnoses (± SDs) per year as well as average sex-specific rates (± SDs) per year of urogenital malignancies in Surinamese men of Hindustani, Creole, and Javanese background in the period between 1980 and 2004. Sex-specific rates are per 100,000 men per year. Discrepancies between the number of overall cases mentioned in Table 1 and the total number of cases given below, were due to the absence of information about the ethnic background of the patients in some cases.

Hindustanis Creoles Javanese

Total Average Average Total Average Average Total Average Average number yearly sex- number yearly sex- number yearly sex- of cases number of specific of cases number specific of cases number specific cases rate of cases rate of cases rate

Prostate 55 2.2 ± 1.7 1 1.0 ± 0.8 1 484 19.4 ± 13.5 9.1 ± 5.7 38 1.5 ± 1.7 1 0.7 ± 0.8 1 Urinary bladder 15 0.6 ± 0.8 1 0.3 ± 0.4 1 34 1.4 ± 1.3 0.7 ± 0.7 11 0.4 ± 0.5 1 0.2 ± 0.2 1 Penis 14 0.5 ± 0.6 1 0.2 ± 0.3 1 27 1.1 ± 0.9 0.5 ± 0.4 5 0.2 ± 0.5 1 0.1 ± 0.3 1 Kidneys 7 0.3 ± 0.5 0.1 ± 0.2 9 0.4 ± 0.6 0.2 ± 0.3 3 0.1 ± 0.3 0.0 ± 0.1 Testes 4 0.2 ± 0.4 0.1 ± 0.2 8 0.3 ± 0.5 0.2 ± 0.2 3 0.1 ± 0.3 0.1 ± 0.2

Total 95 - - 562 - - 60 - -

1Significantly different from ‘Creoles’ (P < 0.001).

Discussion disease in order to recognize causative factors and to improve diagnosis and treatment. In this survey on the incidence of male urogenital malignancies in Suriname, Studies on the epidemiology of cancer aim to almost 900 overall cases have been diagnosed between identify trends and risk factors associated with malignant the years 1980 and 2004. We previously reported the Acad J Sur 2011 (2) 198-204 202 Mans et al.

occurrence of roughly 7,500 cancers overall in the Aging may predispose to cancer due to the country in this period, approximately 40% of which was accumulation of errors in the DNA of target cells over a in males (Mans et al., 2008). Accordingly, male lifetime, as well as age-related alterations in the immune urogenital malignancies comprised about 12% of all and endocrine system (Anisimov et al., 2009; Pawelec et cancers in Suriname, and about 30% of cancers in al., 2010). Accordingly, incidence rates of overall as Surinamese men. Thus, similarly to malignancies of the well as most individual male genitourinary cancers female genitourinary tract – which comprised 1 out of increased markedly with advanced age. This was every 5 overall cancers and almost half of all neoplasms particularly evident for prostatic cancer, that was in women (Mans et al., 2011) – those of the male virtually non-existent in males younger than 50 years, urogenital system were not uncommon in Suriname. but manifested at a frequency of almost 28 new The overwhelming majority of male diagnoses per year (or almost 1 new case every 2 weeks) genitourinary malignancies – almost 90% - originated in men of 50 years and older. This observation is from the genital system. This could be ascribed to the completely in agreement with the general consensus that very high number of prostatic cancers, comprising nearly this malignancy is a disease of advanced age that is 90% of genital neoplasms. Thus, when considering the relatively rare in men under age 55 (Nelen, 2007). The occurrence of about 7,500 cancers overall and 3,000 not insignificant number of testicular and kidney cancer male cancers in Suriname in the period covered by this cases younger than 50 years (about 30%) is in line with study (Mans et al., 2008), it can be concluded that the unusual age-distribution of these neoplasms, prostatic cancer constituted nearly one-tenth of all occurring often in young and middle-aged men (Hayes- malignancies in the country, and almost one-quarter of Lattin and Nichols, 2009), and in children and all neoplasms in Surinamese men. The average sex- adolescents (Perlman, 2005), respectively. specific rate of approximately 13 per 100,000 men per As previously reported for cancer overall and year is well in accordance with values estimated before various individual neoplasms in Suriname (Mans et al., (Mans et al., 2003, 2008). This value is in the range of 2003, 2007, 2008, 2010, 2011), male urogenital those of 8.3 to 16.4 seen in low-incidence areas in malignancies displayed a distinct ethnic distribution, Western Asia, Eastern and Middle Africa, and Melanesia having a predilection for Creoles rather than Hindustanis (Jemal et al., 2011), but much lower than those of 71.1 to and Javanese. This held particularly true for prostatic 104.2 reported for high-incidence countries in the cancer, which is in line with the greater occurrence of Caribbean, Western and Northern Europe, North this neoplasm in African Americans than in USA males America, and Australia/New Zealand (Jemal et al., from other ethnic backgrounds (Brawley et al., 1998; 2011). Thus, despite its relatively frequent occurrence in American Cancer Society, 2005). So far, this pattern Suriname, this country can be characterized as a low- cannot be satisfactorily explained. The apparently incidence area for prostatic cancer. exceptionally low incidence of penile cancer in Javanese The other male genital malignancies, penile and when compared to Creoles and Hindustanis (5 versus 14 testicular cancer, were very rare, occurring at rates of and 48, respectively, out of 67) might be tentatively approximately 1 to 3 new case(s) per 100,000 men per 2 attributed to cultural and religious differences among the years. These frequencies were close to those of three groups: the majority of Surinamese Javanese is approximately 1 for low-incidence countries such as the Muslim who, unlike most Creoles and Hindustanis, USA (Frisch and Goodman, 2000; American Cancer practice circumcision that is believed to protect against Society, 2005; Jemal et al., 2006) and China (Parkin et penile cancer (Aboulafia and Gibbons, 2001; Pow-Sang al., 2005), respectively, and significantly lower than et al., 2002; Madsen et al., 2008). Indeed, this those of 5.5 to 8 (Wabinga et al., 2000; Pow-Sang et al., malignancy is extremely uncommon in societies who 2002; Misra et al., 2004) and 3 to 4.4 (American Cancer which practice circumcision, such as other Muslim Society, 2005; Parkin et al., 2005; Jemal et al., 2006), populations, Jewish groups, and the Ibos of Nigeria respectively, observed in high-risk areas in parts of (Micali et al., 2006; Madsen et al., 2008). Africa and South America. These data indicate that To summarize, the occurrence of male Suriname also represents a region of low risk for penile urogenital malignancies in Suriname ranged from rare and testicular cancer. (e.g. , penile and testicular cancer) to relatively common Only 113 of the 899 malignancies of the male (e.g., prostatic cancer). Nevertheless, the frequency of genitourinary system - 12.6% - originated from kidneys these cancer types was characteristic for a low-incidence and urinary bladder. The sex-specific rate of these country. Most individual urogenital neoplasms neoplasms in Surinamese men (1 to 3 new cases per 2 manifested over 50 years of age, but testicular cancer years) was in the range of values reported for low- was also not uncommon between 20 and 50 years. incidence areas in parts of Africa, Melanesia, Asia, as Prostatic cancer had a clear predilection for Creoles, well as South and Central America (1.5 to 3.5), and while penile cancer seemed particularly rare in Javanese much lower than those of 15 to 21 associated with high- men. It is conceivable that more comprehensive incidence areas in Europe and Northern America (Chow epidemiological studies in the multi-ethnic and multi- et al., 2010; Jemal et al., 2011). Thus, similarly to cultural society of Suriname may help to broaden our prostatic, penile and testicular cancer, Suriname understanding of the etiology of cancer. represented a region of low risk for kidney and urinary bladder cancer in males.

Acad J Sur 2011 (2) 198-204 Incidence of male urogenital cancers in Suriname 203

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