Prostate cancer disparities in Black men of African descent: a comparative literature review of prostate cancer burden among Black men in the United States, Caribbean, United Kingdom, and West Africa

Background African American men have the highest prostate cancer morbidity and mortality rates than any other racial or ethnic group in the US. Although the overall incidence of and mortality from prostate cancer has been declining in White men since 1991, the decline in African American men lags behind White men. Of particular concern is the growing literature on the disproportionate burden of prostate cancer among other Black men of West African ancestry in the Caribbean Islands, United Kingdom and West Africa. This higher incidence of prostate cancer observed in populations of African descent may be attributed to the fact that these populations share ancestral genetic factors. To better understand the burden of prostate cancer among men of West African Ancestry, we conducted a review of the literature on prostate cancer incidence, prevalence, and mortality in the countries connected by the Transatlantic Slave Trade. Results Several published studies indicate high prostate cancer burden in Nigeria and Ghana. There was no published literature for the countries Benin, Gambia and Senegal that met our review criteria. Prostate cancer morbidity and/or mortality data from the Caribbean Islands and the United Kingdom also provided comparable or worse prostate cancer burden to that of US Blacks. Conclusion The growing literature on the disproportionate burden of prostate cancer among other Black men of West African ancestry follows the path of the Transatlantic Slave Trade. To better understand and address the global prostate cancer disparities seen in Black men of West African ancestry, future studies should explore the genetic and environmental risk factors for prostate cancer among this group.


Introduction
In the United States (US), an estimated 30,870 cases of prostate cancer are expected to occur among African American men in 2007, accounting for 37% of all cancers diagnosed in African American men [1]. Between 2000 and 2003, the average annual prostate cancer rate was 60% higher in African American men compared to White men [1]. In addition, African American men have the highest mortality rate compared to any other racial or ethnic group in the US, and 2.4 times higher than in White men. Although prostate cancer incidence and mortality rates have been declining in both African American and White men since 1991, possibly due to improved diagnostic techniques, better screening and improved surgical and radiologic treatments, the rates remain comparably higher among African American men. Why does this disparity continue to exist among African American men in spite of the significant research to eliminate this disparity?
The population-based studies on prostate cancer disparity have traditionally studied African American men only or compared African American men to other racial groups within the US. Although these studies have provided vital insights necessary to understanding the primary differences among the ethnic groups in the US, we are left with more questions than answers. With the problem of prostate cancer disparity persisting, it is crucial that we begin to use new paradigms to examine the problem of prostate cancer disparity from new perspectives. The prospect for a new paradigm/new perspectives emerge with the growing literature on the disproportionate burden of prostate cancer among other Black men (in other parts of the world, other than the US) who are related to African American men through the Transatlantic Slave Trade (TAS) [2][3][4][5][6][7], especially Black men of West African ancestry. Based on the World Health Organization (WHO)'s worldwide cancer data, West African men have much lower prostate cancer incidence and mortality compared to African American men. For example, compared to Nigerian men, African-American men are >10 times likely to develop prostate cancer and 3.5 times likely to die from the disease [8]. On the other hand, Silverberg and Lubera [9] reported high rates of prostate cancer mortality in Martinique, Trinidad & Tobago; while Glover et al. [10]reported high rates of prostate cancer incidence in the predominantly Afro-Caribbean population of Jamaica. Thus the variability in risk and mortality across these populations of West African descent suggests a potential and important influence of environmental/lifestyle factors acting on prostate cancer risk in these already susceptible populations. Can this evolving international data hold the key to our better understanding of the etiology of unequal burden of this disease in African American men?

The Transatlantic Slave Trade (TAS) Relations
Based on the TAS, about 15 million people were transported as slaves from Africa, not counting those who died en-route to the Americas, Caribbean and Europe [7]. The TAS comprised the following three journeys: (1) Outward passage from Europe to Africa carrying manufactured goods; (2) Middle passage from Africa to the Americas/ Caribbean carrying African captives and other commodities; and (3) Homeward passage carrying sugar, tobacco, rum, rice, cotton and other goods back to Europe. These slave routes included diverse countries. The European countries involved in the TAS were Portugal, France, Netherlands, Spain, Denmark, Norway and United Kingdom. Slaves were primarily imported from the African countries -Benin, Nigeria, Ghana, Gambia, Senegal, Mozambique, and Angola. The middle passage took the slaves from Africa to the American and Caribbean countries -Barbados, Cuba, Haiti, Dominican Republic, Netherlands Antilles, Trinidad and Tobago, Jamaica, Brazil, and the US. Most of the slaves ended up in South America or the Caribbean with about 500,000 transported to North America. Unfortunately, most of the slaves in the Caribbean, Central America and South America died while the slave population in North America had higher life expectancy [7].

Objective
In this manuscript, we explored the burden of prostate cancer among the TAS population targeting Black men of West African Ancestry to answer the question:Does the prostate cancer disparities seen in Black men around the world follow the path of the TAS?

Methods
To achieve the objective for this study, we conducted a literature review, summarizing the body of evidence on prostate cancer morbidity and mortality in countries with high population of Black men of West African ancestry, excluding the US. Our goal was not to provide a metaanalysis evaluation nor conduct a comprehensive review/ critique of these studies. Our aim was to merely examine the available proof in an effort to better understand the burden of prostate cancer among Black men of West African ancestry. The study countries for our review were West African TAS populations (Benin, Nigeria, Ghana, Gambia, and Senegal), the United Kingdom and Caribbean Islands (Barbados, Cuba, Haiti, Dominican Republic, Netherlands Antilles, Trinidad and Tobago, Jamaica, and Brazil). A systematic search of the computerized database, MEDLINE, was conducted for each country from the originating date of MEDLINE to July 2008 using the following keywords: Black men, prostate cancer, prostate cancer risk, prostate cancer incidence; prostate cancer morbidity; and name of TAS country. The inclusion criteria were: • Original studies and review articles; • Publication in English; • Relevance to prostate cancer risk, incidence, prevalence or mortality; and • Sufficient quality and quantity of evidence based on study design and validity, for example, well designed randomized/non-randomized study with good evidence to support study conclusion.
Studies employing the World Health Organization (WHO) GLOBOCAN program of the International Agency for Research in Cancer (IARC) [11] were excluded from the review because the data from developing countries are unreliable. As noted in the GLOBOCAN 2002 report [11], several developing countries do not have available data for cancer incidence and mortality. Thus, data from neighboring countries in the same regions were used to estimate developing countries. For example, the incidence data for each West African country were estimated from the proportions of available data from the respective country as well as un-weighted averages of the observed rates (by sex and age-group) in registries from other West African countries. The cancer mortality for these countries was calculated as the product of incidence and the probability of dying from the disease. The pooled estimates of survival for the West African regions were applied to countries in these regions. Given the lack of reliable and valid cancer incidence and mortality data for most of the developing countries, the prostate cancer rates reported in the Globocan 2002 report [11] for these countries are underestimated.
The steps for the literature review were in the following order: Step 1 Search for relevant articles using specified keywords on MEDLINE; Step 2 Screening of Titles to eliminate irrelevant articles; Step 3 Screening of abstracts of all articles identified in Step 2 for relevance; and Step 4 Review of papers identified in Step 3 based on inclusion criteria by study investigators. Only the studies with study design ranked Excellent, Good or Satisfactory by authors were included in the review. Subsequently, the studies were grouped together and summarized according to TAS country. It is important to note that some of the studies included more than one (1) TAS country.

Results
Results are presented for each region below.

Tracing the root of prostate cancer disparities to West Africa
The lack of population-based cancer registries in developing countries, especially African countries, leaves only hospital-based prostate cancer morbidity and mortality data. Thus, most of the articles identified in our review presented only hospital-based data. There was no published study on prostate cancer morbidity and mortality in Benin, Gambia, and Senegal. Although there was no published study reporting prostate cancer morbidity and mortality in Senegal, Gueye et al. [12] found the clinical characteristics of prostate cancer among the Senegalese (median PSA of 37.0 ng/mL) to be different from American Blacks (median PSA of 6.3 ng/mL) and Whites (median PSA of 6.1 ng/mL); p < 0.001. Senegalese men had worse median (and mean) PSA level and worse tumor stage. As noted by the authors, these differences can possibly be explained by the considerable differences in early detection between US men and Senegalese men.
Reports on prostate cancer patterns in Ghanaian men were found in only two published studies. The first study was a review of the genitourinary cancers seen at the Accra Korle-Bu Teaching Hospital, Klufio [13]. The authors found prostate cancer to comprise about 64% (349 cases) of all genitourinary cancers from 1980 to 1990. In a more recent study, Wiredu and Armah [14] conducted a 10-year review (1991-2000) of all cancer mortality patterns at the same institution based on autopsy and death certification data, and found prostate cancer to be the second leading cause of cancer deaths (286 cases). None of the studies presented the actual incidence, prevalence or mortality from prostate cancer.
Contrary to the WHO IARC global ranking, several published studies indicate higher incidence of prostate cancer in Nigerian men. A total of 17 original papers, which met our review criteria, were found to document prostate cancer patterns in Nigeria. Odedina, Ogunbiyi and Ukoli previously reviewed all the 17 articles in 2006 [8]. The first published paper reviewed by Odedina, Ogunbiyi and Ukoli [8] was as early as 1981 and the latest study in 2005. The studies were conducted in different regions of Nigeria, including the North, Southeast, West, and in rural South. The authors concluded that the body of evidence from the 17 studies indicates high prostate cancer risk among Nigerian men and a prostate cancer burden similar to that of Black men in the US. Table 1 provides a summary of the prostate cancer incidence and prevalence rates reported in the review article.   [20] also reported that prostate cancer continued to be the leading cancer mortality site among Jamaican men.

Tracing the root of prostate cancer disparities to Caribbean Islands
The three published studies found to be relevant for Trinidad and Tobago were by Bunker et al. [21][22][23]. In 2004, Bunker at al [21] reported a population-based prostate cancer study, screening on about half the population of Tobago men. Over 2,500 men between the age of 40 and 79 years were screened using serum prostate-specific antigen (PSA) and digital rectal examination (DRE). The authors found biopsy-confirmed prostate cancer prevalence in this population to be about 11% (277 out of 2,583 men). These results confirmed the findings of an earlier report on the same population by Bunker et al. [22] based on the screening of 2,484 men between the age of 40 and 79 in Tobago. In another report, Bunker et al. [23] compared the Tobago population of West African descent to the men of Asian-Indian descent in Trinidad, targeting men between 50 and 64. The prostate cancer prevalence based on population-based screening was found to be significantly higher for the Afro-Tobagonian men (8.3%) compared to the Asian-Indian men (2.3%). This differ-ence was also observed on all age categories: 50-54; 55-59; and 60-64.

Tracing the root of prostate cancer disparities to United Kingdom
The populations of Black men in the United Kingdom (UK) provide a very interesting population to study because they are mostly Afro-Caribbean and West African men. Thereby, they uniquely reflect a microcosm of the West African and Caribbean populations described above. men. As noted by the authors, this risk is more than the risk documented for African American men in the US. A reason that has been suggested for the larger relative difference between African-Caribbean and European men is a lower prostate cancer rate for White men in the UK [25].
In a follow-up study published this year, the PROCESS study group [25] [24]. An interesting component of the current study is the comparison of the Black Caribbean group to the Black African group, with no statistically significant difference on age-adjusted prostate cancer rates between both groups.

Discussion and conclusion
Based on the growing literature on the disproportionate burden of prostate cancer among other Black men of West African ancestry, it is clear that this clearly follows the path of the TAS. The primary West African source populations for the TAS were the African countries -Benin, Nigeria, Ghana, Gambia and Senegal. Our critical review of the literature on these West African countries found that the true prostate cancer rates reported for West Africans by the WHO [11] may be underestimated. This is not surprising since there are no data available on cancer incidence and mortality for most of the West African countries. Contrary to the global ranking, several published studies, including our previous review article for Nigeria [8], indicate higher incidence of prostate cancer in Nigeria [26][27][28][29][30][31][32][33][34][35][36][37][38][39][40] and Ghana [13,14]. There are no published literature for Benin, Gambia and Senegal. Prostate cancer morbidity and/or mortality data from the Caribbean Islands [10,[15][16][17][18][19][20][21][22][23] and the UK [24,25] also provide similar or worse prostate cancer burden for Black men of West African ancestry.   Table 1 provides a summary of the numerical findings of published incidence and prevalence rates for prostate cancer in Black men of West African Ancestry. It is worth noting that the direct comparisons of these numerical findings may not be valid given the differences in the data reporting methods for the incidence and prevalence of, and mortality from prostate cancer in these countries. The validity of the data reporting methods are further limited in African countries due to underreporting [26], lack of appropriate diagnosis [26,27,37,41], limited access to care [41], differences in technical manpower and infra-structure [41], and the quality of cancer data systems [41][42][43][44][45].
The consistent higher incidence of prostate cancer relative to other groups, observed in populations of West African descent may be attributed to the fact that these populations share ancestral genetic factors that increase susceptibility to prostate cancer. However, the likely variability in risk across these populations of African men around the world may also suggest a potential and important influence of environmental/lifestyle factors acting on prostate cancer risk in these susceptible populations.

Competing interests
The authors declare that they have no competing interests. cles on the burden of prostate cancer in the Caribbean ancestral groups of U.S. Black men. All the authors reviewed and approved the manuscript.