High Prevalence of Screening-detected Prostate Cancer among

Afro-Caribbeans: The Tobago Prostate Cancer Survey

Clareann H. Bunker,2 Alan L. Patrick, Badrinath R. Konety, Rajiv Dhir, Adam M. Brufsky, Carlos A. Vivas, Michael J. Becich, Donald L. Trump, and Lewis H. Kuller

Departments of Epidemiology [C. H. B., A. L. P., L. H. K.], Medicine [A. M. B., D. L. T.], Urology [B. R. K., C. A. V.], and Pathology [R. D.,

M. J. B.], University of Pittsburgh, Pittsburgh, Pennsylvania 15261

Risk for prostate cancer is high among African Americans. We hypothesized that risk for prostate cancer is also high in other populations of African descent. Our objective was to determine the screening-detected prevalence of prostate cancer in the predominantly Afro- Caribbean population on the island of Tobago.

Male residents, ages 40–79 years, were invited to participate in a population-based screening for prostate cancer using serum prostate-specific antigen (PSA) and digital rectal exam (DRE). Men with elevated PSA (>4 ng/ml) or abnormal DRE were offered an ultrasound-guided sextant biopsy of the prostate gland. Men (2484), ages 40–79 years, underwent prostate cancer screening between September 1997 and June 2001. Mean age was 55.9, SD was 10.6 years, and median was 54 years. Mean serum PSA was 14.8 ng/ml, SD was 376 [excluding 4 values > 2 SD above the mean (1,112, 1,317, 1,818, and 18,330 ng/ml) mean PSA was 5.5 ng/ml and SD was 29.6], and median PSA was 1.2 ng/ml.

Elevated PSA and/or abnormal DRE were observed in 31% (759 of 2484) overall, and in age groups 40–49 (87 of 843, 10%), 50–59 (201 of 729, 28%), 60–69 (262 of 584, 45%), and 70–79 (209 of 328, 64%). Of 681 men biopsied, 259 (38%, or 10% of the 2484 screened) were diagnosed with prostate cancer. Age-specific rates of screening detected prostate cancer were: 1%, ages 40–79 years; 7%, ages 50–59 years; 18%, ages 60–69 years; and 28%, ages 70–79 years.

These screening results indicate a very high screening-detected prevalence of prostate cancer in this population of West African descent. These data support the hypothesis that populations of African descent share genetic and/or lifestyle factors that contribute to their elevated risk for prostate cancer.

Introduction

Prostate cancer is a very serious personal and public health

problem affecting African Americans more frequently than

Caucasians. On the basis of 1990–1997 data from the U.S.

SEER4 of the National Cancer Institute (1), age-adjusted incidence

of prostate cancer is 225 of 100,000 among African

Americans compared with 149 of 100,000 among white non-

Hispanics. The mortality rate from prostate cancer was  2-fold

higher among persons of African descent (54 of 100,000)

compared with white non-Hispanics (23 of 100,000). Incidence

of prostate cancer in the United States increased dramatically in

both groups between the late 1980s and 1993, reflecting the

earlier diagnosis that occurred with the increasing use of serum

PSA screening (1). An encouraging downturn in prostate cancer

mortality rates was observed in both ethnic groups from 1993

to 1997 (1).

Established risk factors for prostate cancer include age,

ethnicity, family history of prostate cancer, and high-fat or meat

diet (2). Other factors suspected include hormone metabolism,

(3, 4) vitamin D metabolism, (5) and a few occupational exposures

(6). The relationships of a number of candidate genes

to prostate cancer are under investigation with most published

results limited to Caucasian populations (7, 8). The reasons for

the higher risk for prostate cancer among African Americans

are unknown.

Until recently, there has been little solid prevalence, incidence,

or mortality data for populations of African descent

outside the United States, although data published a few years

ago in an annual summary of worldwide data suggested high

rates of prostate cancer mortality in Martinique and Trinidad &

Tobago (9). Glover et al. (10) reported high rates of prostate

cancer incidence in the predominantly Afro-Caribbean population

of Jamaica. Data regarding screening parameters and prevalence

of prostate cancer in populations of African descent in

the United States are sparse (11, 12) and virtually absent in

other populations of African descent. However, a recent publication

has estimated prostate cancer prevalence for 1994

among African Americans and Caucasians using a model based

on incidence and survival functions calculated from the Connecticut

Tumor Registry, 1940–1993, and applied to the SEER

1973–1993 populations. The prevalence proportion ranged

from 7 of 100,000, ages 40–44 years, to 9,725 of 100,000, ages

Received 8/16/00; revised 4/1/02; accepted 4/22/02.

726 Vol. 11, 726–729, August 2002 Cancer Epidemiology, Biomarkers & Prevention

75–79 years, in Caucasians, compared with 14 of 100,000, ages

40–44 years, to 10,945 of 100,000, ages 75–79 years, in

African Americans (13).

We hypothesize that risk for prostate cancer is high among

populations of African descent living in diverse environments.

If so, this would lead us to hypothesize that populations of

African descent share genetic and/or lifestyle factors that increase

risk for prostate cancer.

On the island of Tobago, Trinidad & Tobago, we are

conducting a population-based, longitudinal study of prostate

cancer in the male population ages 40–79 years. In this report,

we present data from the initial cross-sectional screening using

serum PSA and DRE.

Materials and Methods

Population. The island of Tobago is about 7  26 miles in

size. According to the 1990 census (14) of Trinidad & Tobago,

the male population of Tobago, ages 40–79 years, numbered

5121. Ninety-two percent of Tobago residents reported that

they were of African descent. Most healthcare is provided by a

government-supported system through the Tobago Regional

Health Authority that manages the 19 neighborhood health

centers and one hospital. Some residents travel to Trinidad for

specialized care under the government system. Some care is

provided by private caregivers. PSA testing has been available

but generally limited to symptomatic men seeking care in the

private sector.

Recruitment. The recruitment goal was 4000 men, 80% of the

male population of Tobago, ages 40–79 years. Currently,

3000 men are enrolled. Recruitment has been the result of

word of mouth, informing by healthcare workers at the hospital

and health centers, informing by private physicians, posters,

flyers, public service announcements, and public presentations

by oncologists and urologists from Trinidad and the United

States.

Informed Consent. Consent was obtained using forms and

procedures approved by the Institutional Review Boards of

University of Pittsburgh Institutional Review Board and the

Tobago Ministry of Health.

Data Collection. Data were collected by locally resident study

staff at the study office located at the Tobago Regional Hospital.

Data collected included ethnicity, education, occupation,

smoking, medical history, personal and family cancer history,

vasectomy, prostate symptoms, health screening history, alcohol

intake, detailed occupational history, and height, weight,

waist, and hip measurements.

Biological Sample Collection. A 15-ml plain vacutainer of

peripheral blood was drawn from fasting subjects. Aliquots of

serum were frozen at 20°C for later measurement of PSA.

DRE. A systematic DRE was performed by a physician trained

according to the study protocol. This exam was scheduled after

the blood draw to avoid an artifactual increase in serum PSA

that may follow digital manipulation of the gland.

PSA Measurement. Serum PSA levels were measured at the

University of Pittsburgh Central Pathology Laboratory using

the automated Microparticle Enzyme Immunoassay, Abbot Ax-

SYM PSA assay (Abbott Laboratories, Abbott Park, IL).

Criteria for Referral for Prostate Biopsy. Subjects were

referred to the Tobago Regional Hospital for biopsy if the DRE

was abnormal (except for simple enlargement without palpably

abnormal areas) or if serum PSA was elevated (4.0 ng/ml).

Prostate Biopsy. Prostate biopsies were performed by urologists

or by surgeons trained by urologists from the University of

Pittsburgh Medical Center. Trans-rectal ultrasound guided biopsy

was performed using an 18 gauge, 21-cm spring-loaded

biopsy needle (Boston Scientific, Natick, MA). Sextant biopsies

were obtained according to a standard protocol.

Prostate Pathology. The formalin preserved specimens were

stored at room temperature and shipped to the University of

Pittsburgh for histopathological examination. The specimens

were examined for presence or absence of high-grade prostatic

intraepithelial neoplasia, presence or absence of cancer, Gleason

score of cancer, location of cancer, and perineural invasion.

Data Analysis. Age-specific prevalence rates (per 100

screened men) were calculated. Age-adjusted rates/100 and

SE/100 were calculated by direct standardization (15) based on

the age distribution (50–79 years) of the 1970 United States

standard million population (1). Positive predictive value of the

screening tests was calculated as number of men diagnosed

with prostate cancer divided by the number of men with abnormal

DRE and/or elevated PSA who underwent biopsy. All

statistical calculations were performed using SPSS 10.0 for

Windows (SPSS Inc., Chicago, IL).

Results

PSA and/or DRE screening was completed for 2492 men, ages

40–79 years, 49% of the total male population in this age

group. Eight men who reported prior diagnosis of prostate

cancer are excluded from these analyses. Among the 2484 men

remaining, mean age was 55.9 years, SD was 10.6, and median

was 54 years. Ninety-two percent of men reported three or four

grandparents of African descent, whereas 5% reported one or

two of African descent. Twenty-four percent had completed

secondary school or higher education. Forty-two percent reported

ever smoking, whereas 14% were current smokers.

The serum PSA range was 0.1–18,330 ng/ml. Mean serum

PSA was 14.8 ng/ml and SD was 376. After excluding 4

values  2 SD above the mean [1,112, 1,317, 1,818, and 18,330

ng/ml], mean PSA was 5.5 ng/ml, SD was 29.6, median PSA

was 1.2 ng/ml, and range was 0.1–602 ng/ml.

Elevated serum PSA levels (4 ng/ml) were observed in

452 of 2437 men (19%), ranging from 2% of men, ages 40–49

years, to 53% of men, ages 70–79 years. DRE was abnormal in

514 of 2074 men (25%). Frequency of abnormal DRE increased

across age groups from 11 to 48%. Abnormal screening results

(PSA  4 ng/ml and/or abnormal DRE) are shown in Table 1.

PSA and/or DRE were abnormal in 759 of 2484 men (31%).

Thus, a high proportion of the screened men was referred for

biopsy: 10% of men, ages 40–49 years; 28%, ages 50–59

years, 45%, ages 60–69 years; and 64%, ages 70–79 years.

Of the 759 men referred for biopsy, 681 (90%) have

undergone prostate biopsy. Prostate cancer was diagnosed in

259 (38%) men, 2 (1%) with Gleason grade 5, 142 (55%) with

grade 6, 86 (33%) with grade 7, and 29 (11%) with grades 8, 9,

and 10. The prevalence of prostate cancer among screened men

was 10% (259 of 2484) among men ages 40–79 years, and 15%

(250 of 1585) among men ages 50–79 years. The age specific

results are shown in Table 1.

The high prevalence rate reported above reflects not only

the high rate of abnormal screening results but also a highpositive

predictive value for an abnormal screen: 12% of biopsied

men ages 40–49 years were diagnosed with prostate cancer;

27%, ages 50–59 years; 45%, ages 60–69 years; and 53%,

ages 70–79 years (Table 1).

Among 123 men reporting family history of prostate cancer,

117 reported one relative, 5 reported two relatives, and 1

reported three relatives with prostate cancer. The distribution of

727 Cancer Epidemiology, Biomarkers & Prevention

relatives included 78 fathers, 65 brothers, 3 half-brothers, 8

uncles, and 2 grandfathers. Thirteen (10.6%) of 123 men reporting

family history of prostate cancer were diagnosed with

prostate cancer, compared with 246 (10.4%) men diagnosed

with prostate cancer among 2361 men not reporting family

history of prostate cancer.

Eight percent of men reported that a physician had told

them they had benign prostatic hypertrophy. Waking to urinate

more than once/night was reported by 51% of men (62% of men

ages 50–79 years). The rate rose steadily from 33% among men

ages 40–49 years to 86% among men ages 70–79 years. Within

each age group, the rate was similar in cases and noncases.

Discussion

The screening detected prevalence of prostate cancer in this

Afro-Caribbean population, ages 50–79 years, was about three

to four times higher than rates reported from screening studies

of predominantly Caucasian populations (16–18). These

United States studies, which reported results by age group, were

conducted between 1989 and 1992 when PSA screening was

just beginning to be widely used in the United States. After

direct age adjustment to the standard 1970 United States population,

ages 50–79 years (SEER), screening-detected prevalence

in Tobago men, ages 50–79, was 15.1 of 100, SE 0.9,

compared with 3.8 of 100, SE 0.2, in a population of 6501

United States men (92% Caucasian, 3% African American, and

5% other), ages 50–79 years, reported by Richie et al. (18).

Comparison of the age-specific screening-detected prevalence

rates of prostate cancer in these two populations are shown in

Fig. 1.

Factors that may influence the comparison of the screening

results from these two populations include the biopsy protocol,

the proportion of men with abnormal PSA/DRE who underwent

biopsy, prior level of screening in the populations, and recruitment

methods. In the study by Richie et al. (18), quadrant

ultrasound guided needle biopsies were performed, whereas

this study required sextant biopsies, which were likely to have

resulted in some increase in the probability of detecting cancer

if cancer was present (19). The biopsy rate among men with

abnormal screening results was 90% in the Tobago study,

compared with 69% in the study by Richie et al. (18). This

higher biopsy rate increased the opportunity to ascertain cases.

Thus, procedural differences may account for some of the

increased prevalence rate among the Tobago men.

The United States population in the previously mentioned

study (18) was screened in 1991–1992, a period during which

the incidence of prostate cancer was rising sharply (1), reflecting

increasing use of PSA testing. Thus, some prostate cancer

cases may have been removed from this United States population

by prior screening. However, 19% of the Tobago men, ages

50–79 years, reported a prior PSA test, suggesting that some

level of screening had also been available in this Tobago

population.

Both the United States (18) and the Tobago populations

were self-referred. The Tobago population was recruited primarily

by word of mouth. The United States population was

recruited by advertisement. Among the United States population,

53% reported symptoms of prostatism. Sixty-two percent

of Tobago men, ages 50–79 years, reported waking to urinate

two or more times/night. If self-referral bias were to have a

strong effect, one would have expected higher prostate cancer

rates among men recruited earlier in the study compared with

later. As shown in Fig. 2, this was somewhat true, particularly

in the oldest age group among whom symptoms were more

likely to be related to prostate cancer. Compared with the

age-standardized rate of screening-detected prostate cancer

(15.1%) among men ages 50–79 years in the total screened

group, the rate based on the men recruited only in 2000–2001

was somewhat lower, 13.4%. Even after deflating the conservative

13.4% rate by the ratio of the biopsy rates in the two

populations, the even more conservative estimate of the agestandardized

rate of screening-detected prostate cancer of

10.3% is still almost 3-fold higher than in the United States

population, Richie et al. (18).

Similar age-specific prevalence rates from screening of

other populations of African descent have not been published.

Fig. 1. Screening detected prevalence of prostate cancer among 6501 predominantly

Caucasian United States men (18) and 2484 Afro-Tobagonian men.

Table 1 Screening and biopsy results in Tobago men by age group

Age

group (yr)

Screened

n

Abnormal DRE

and/or PSA n

(% of screened)

Biopsied n (%

of abnormal)

Prostate cancer n

(% of biopsied)

Prostate cancer prevalence

(per 100 screened population)

40–49 843 87 (10) 77 (89) 9 (12) 9/843 (1)

50–59 729 201 (28) 188 (94) 50 (27) 50/729 (7)

60–69 584 262 (45) 240 (92) 107 (45) 107/584 (18)

70–79 328 209 (64) 176 (84) 93 (53) 93/328 (28)

Total age 2484 759 (31) 681 (90) 259 (38) 259/2484 (10)

40–79

Total age 1641 672 (41) 604 (90) 250 (41) 250/1641 (15)

50–79

728 High Prostate Cancer Prevalence in Afro-Caribbeans

Smith et al. (20) reported prostate cancer prevalence of 5.1%

among 804 African-American men screened between 1991 and

1995 using serum PSA and DRE. Application of the Tobago

prostate cancer rates to the reported age distribution in this

African-American population yielded an expected rate of

12.4%, compared with the observed prevalence of 5.1%, suggesting

that the Tobago rates are approximately twice those

observed in the African-American population.

One of the known risk factors for prostate cancer is ethnicity,

i.e., African descent, although we do not know how this

risk is mediated. One hypothesis is that genetic factors contribute

to the high risk for prostate cancer among populations of

African origin. If the Caucasian admixture rate in the Tobago

population is indeed low, then this population may carry a

higher burden of high-risk genes of African descent than the

more admixed populations in the United States.

In conclusion, compared with Caucasian and other populations,

the higher incidence of prostate cancer observed in

populations of African descent, African Americans (1) and

Jamaicans (10), and the very high screening-detected prevalence

of prostate cancer observed in this study among Tobagonians

support the hypothesis that these populations share ancestral

genetic factors that increase susceptibility to prostate

cancer. However, the variability in risk across these populations

of African descent suggests an important influence of unknown

environmental/lifestyle factors acting on prostate cancer risk in

these susceptible populations.