Skip to main content
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2014 Oct 1.
Published in final edited form as: Cancer Causes Control. 2013 Jul 17;24(10):1893–1899. doi: 10.1007/s10552-013-0257-2

Diabetes and prostate cancer screening in black and white men

Maureen Sanderson 1, Jay H Fowke 2, Loren Lipworth 2, Xijing Han 3, Flora Ukoli 4, Ann L Coker 5, William J Blot 2,3, Margaret K Hargreaves 6
PMCID: PMC3773007  NIHMSID: NIHMS506731  PMID: 23860952

Abstract

Purpose

Prior studies conducted primarily among white men, find a reduced risk of prostate cancer associated with time since developing diabetes. While biologic explanations are plausible, the association may in part arise from more frequent prostate cancer screening among those with a diabetes diagnosis. The purpose of the present study was to investigate the association between diabetes and prostate cancer screening.

Methods

We examined differences in prostate cancer screening (prostate-specific antigen and/or digital rectal examination) testing practices after a diabetes diagnosis among lower-income persons living in the southeastern United States and enrolled in the Southern Community Cohort Study between 2002 and 2009. Baseline in-person interviews collected information on history of diabetes and prostate cancer screening from 18,809 black and 6,404 white men aged 40-79 years.

Results

After adjustment for confounding, diabetic black (odds ratio (OR) 1.12, 95% confidence interval (CI) 1.01-1.25) and white (OR 1.25, 95% CI 1.03-1.51) men were more likely to undergo recent prostate cancer screening compared to non-diabetic men of the same race. The increased risk for prostate cancer screening, however, occurred primarily within the first 12 months after diabetes diagnosis.

Conclusions

Our results suggest that a diabetes diagnosis modestly increases the likelihood of having a prostate cancer screening test for both black and white men. The prevalence of screening was higher nearer to the time of diabetes diagnosis, which may contribute to an early increase in prostate cancer detection followed by lower prostate cancer detection after an extended time.

Keywords: Race, prostate cancer screening, diabetes, cohort study

Introduction

Increasing evidence suggests that diabetes is associated with reduced prostate cancer risk [1-3], with a summary relative risk (RR) of 0.84 (95% confidence interval (CI) 0.76-0.93) in a published meta-analysis [3]. However, two large prospective studies, the Cancer Prevention Study II [1] and Health Professionals Follow-up Study [2], found that prostate cancer risk initially increased for 3 years (RR=1.2) and 1 year (RR=1.3), respectively, following a diabetes diagnosis, before decreasing with longer time since diabetes diagnosis (RR=0.63 and RR=0.75-0.82). Possible explanations for an inverse association between diabetes and prostate cancer include a direct effect of diabetes on reduced prostate cancer growth by lowering insulin [3] or bioavailable testosterone [4] levels, a secondary effect of diabetes drugs such as metformin on prostate carcinogenesis [5], or alternatively an indirect effect due to changes in prostate cancer screening after diabetes diagnosis [6].

Few studies have included black men [3], despite greater diabetes and prostate cancer burdens compared to white men. In the Multiethnic Cohort Study (MEC), a weaker reduction in prostate cancer risk was observed among black (RR=0.89) than white (RR=0.65) men followed for eight years after diabetes diagnosis, despite similar PSA screening frequency by diabetes status in both groups [7]. A cohort study of United States (US) veterans, conducted before the introduction of prostate-specific antigen (PSA) screening, observed similar reductions in prostate cancer risk associated with diabetes among black (RR=0.91) and white (RR=0.88) men, with median follow-up time of 10.5 years for diabetics and 11.9 years for non-diabetics [8].

We investigated the relationship between diabetes and prostate cancer screening, in an attempt to determine its mediating effect on the diabetes and prostate cancer association. Several studies have shown reduced breast cancer screening among diabetic women, but no study has evaluated the association between diabetes and timing of prostate cancer screening. We wished to assess the possibility that decreased prostate cancer screening among diabetics, as seen with the association between diabetes and breast cancer screening, may partially explain the observed reduced risk of prostate cancer associated with diabetes. We hypothesized that prostate cancer screening would be most prevalent near the time of diabetes diagnosis, and, to explain the stronger reduction in prostate cancer risk associated with diabetes among white than black men seen in the MEC [7], that white diabetic men would undergo prostate cancer screening more frequently than white non-diabetic men. In contrast, there would be no association between diabetes and prostate cancer screening among black men.

Methods

Detailed methods of the Southern Community Cohort Study (SCCS), which enrolled black and white men and women in the southeastern US aged 40-79 years, appear elsewhere [9]. Approximately 85 percent of participants completed in-person interviews at the time of enrollment at Community Health Centers (CHC), with the remainder recruited through general population sampling and completion of mailed questionnaires. After exclusion of men of other racial/ethnic groups, men with a history of any cancer or a severe comorbidity (e.g., HIV/AIDS, chronic obstructive pulmonary disease, and history of myocardial infarction) that would preclude screening, and men whose PSA/digital rectal exam (DRE) screening history was not available, the study population for the current analysis comprised 18,809 black and 6,404 white men.

Men were classified as diabetic at baseline if they reported being told by their doctor they had diabetes or high blood sugar, and were further characterized by time since diabetes diagnosis (<1-year, then 5-year categories), year of diagnosis (pre- and post-1994), and use of diabetes medications (oral, insulin). PSA and/or DRE screening was categorized as having occurred within the past 12 months. We stratified by race rather than assess it as an effect modifier because the MEC study reported a stronger association between diabetes and prostate cancer among white than among black men [7]. Covariates of interest included: age, annual household income, educational level, marital status, health insurance coverage, recruitment source, body mass index (BMI, kg/m2) at age 21 years and maximum, hypertension, cholesterol medication use (previously associated with PSA testing) [10], smoking, and leisure-time moderate and vigorous physical activity during their 30s in hours per week, all self-reported on the baseline questionnaire and categorized as in Table 1. Based on previous studies of diabetes and prostate cancer, age [2, 8] and maximum BMI [2, 8] were assessed as effect modifiers of the diabetes and prostate cancer screening association prior to being assessed as confounders, as were marital status and health insurance, both of which are strong predictors of prostate cancer screening in these data [11].

Table 1. Demographic characteristics of men who were and were not screened for prostate cancer within the past 12 months, Southern Community Cohort Study, 2002-2009.

Screeneda Not screened

Characteristic n % n % p-value

Black Men
Age (years) <0.0001
 40-44 711 16.6 4341 31.7
 45-49 931 21.7 3751 27.4
 50-54 980 22.9 2833 20.7
 55-59 713 16.7 1521 11.1
 60-64 504 11.8 708 5.2
 65-69 256 6.0 326 2.4
 70-74 134 3.1 151 1.1
 75-79 54 1.3 64 0.5
Annual household income <0.0001
 <$15,000 2065 48.9 8321 61.3
 $15,000-$24,999 885 21.0 3045 22.4
 $25,000-$49,999 726 17.2 1581 11.7
 $50,000-$99,999 420 9.9 507 3.7
 ≥$100,000 128 3.0 115 0.9
Educational level <0.0001
 <9 years 355 8.3 1009 7.4
 9-11 years 812 19.0 3572 26.1
 Completed high school or GED 1372 32.1 5263 38.5
 Vocational/Some college 1085 25.3 2936 21.5
 Graduated from college 390 9.1 657 4.8
 Graduate school 267 6.2 250 1.8
Marital status <0.0001
 Single 956 22.5 4790 35.1
 Married/living with a partner 1729 40.7 3856 28.2
 Divorced/widowed/separated 1560 36.8 5015 36.7
Health insurance coverage <0.0001
 None 1436 33.7 7482 54.8
 Medicare/Medicaid only 1123 26.3 2827 20.7
 Any private/CHAMPUS/other 1709 40.0 3337 24.5
Recruitment source <0.0001
 Community Health Centers 3613 84.4 12941 94.5
 General population 670 15.6 754 5.5
Body mass index (kg/m2) at age 21 0.03
 <18.5 284 7.0 953 7.3
 18.5-24.9 2428 59.7 8088 61.8
 25-29.9 1058 26.0 3081 23.6
 30-34.99 224 5.5 681 5.2
 35-39.99 51 1.3 178 1.4
 40 24 0.6 101 0.8
Body mass index (kg/m2) maximum <0.0001
 <20 25 0.6 137 1.0
 20-24.99 578 13.8 2684 19.9
 25-29.99 1468 35.0 4848 35.9
 30-39.9 1771 42.3 4872 36.1
 40 350 8.4 959 7.1
Hypertension <0.0001
 No 1652 38.6 7736 56.5
 Yes 2630 61.4 5954 43.5
Cholesterol medications <0.0001
 No 3464 81.3 12564 91.8
 Yes 797 18.7 1117 8.2
Smoking <0.0001
 Never 1144 26.9 2997 22.0
 Former 1160 27.3 2214 16.2
 Current 1944 45.8 8427 61.8
Moderate physical activity during their 30s (hours per week) 0.12
 0 244 5.9 916 6.8
 0.01-2.00 56 1.3 171 1.3
 2.01-4.99 69 1.7 255 1.9
 ≥5 3802 91.2 12160 90.1
Vigorous physical activity during their 30s (hours per week) 0.20
 0 397 9.5 1340 9.9
 0.01-2.00 182 4.4 494 3.7
 2.01-4.99 134 3.2 434 3.2
 ≥5 3463 82.9 11247 83.2

White Men

Age (years) <0.0001
 40-44 152 8.0 1169 27.8
 45-49 261 13.6 1090 26.0
 50-54 348 18.2 758 18.0
 55-59 428 22.4 577 13.7
 60-64 360 18.8 334 8.0
 65-69 222 11.6 161 3.8
 70-74 99 5.2 85 2.0
 75-79 43 2.3 27 0.6
Annual household income <0.0001
 <$15,000 441 23.6 1922 46.2
 $15,000-$24,999 222 11.9 787 18.9
 $25,000-$49,999 382 20.5 683 16.4
 $50,000-$99,999 525 28.1 515 12.4
 ≥$100,000 298 16.0 253 6.1
Educational level <0.0001
 <9 years 102 5.3 316 7.5
 9-11 years 144 7.5 656 15.6
 Completed high school or GED 433 22.7 1400 33.4
 Vocational/Some college 467 24.5 1034 24.6
 Graduated from college 372 19.5 427 10.2
 Graduate school 392 20.5 364 8.7
Marital status <0.0001
 Single 153 8.4 764 18.4
 Married/living with a partner 1271 69.3 1889 45.6
 Divorced/widowed/separated 409 22.3 1493 36.0
Health insurance coverage <0.0001
 None 350 18.4 2043 48.8
 Medicare/Medicaid only 281 14.8 739 17.7
 Any private/CHAMPUS/other 1272 66.8 1405 33.6
Recruitment source <0.0001
 Community Health Centers 887 46.4 3217 76.6
 General population 1026 53.6 984 23.4
Body mass index (kg/m2) at age 21 0.04
 <18.5 103 5.5 254 6.2
 18.5-24.9 1165 62.6 2480 60.3
 25-29.9 478 25.7 1067 25.9
 30-34.99 92 4.9 223 5.4
 35-39.99 11 0.6 63 1.5
 40 13 0.7 29 0.7
Body mass index (kg/m2) maximum <0.0001
 <20 7 0.4 27 0.7
 20-24.99 182 9.7 599 14.4
 25-29.99 697 37.0 1458 35.1
 30-39.9 819 43.5 1673 40.3
 40 179 9.5 394 9.5
Hypertension <0.0001
 No 942 49.2 2586 61.6
 Yes 971 50.8 1614 38.4
Cholesterol medications <0.0001
 No 1309 68.8 3622 86.5
 Yes 593 31.2 567 13.5
Smoking <0.0001
 Never 685 36.5 1031 24.8
 Former 789 42.1 1033 24.8
 Current 402 21.4 2102 50.5
Moderate physical activity during their 30s (hours per week) <0.0001
 0 92 5.0 281 6.8
 0.01-2.00 26 1.4 62 1.5
 2.01-4.99 80 4.4 100 2.4
 ≥5 1635 89.2 3672 89.2
Vigorous physical activity during their 30s (hours per week) <0.0001
 0 180 9.8 447 10.9
 0.01-2.00 116 6.3 155 3.8
 2.01-4.99 111 6.1 124 3.0
 ≥5 1427 77.8 3392 82.4
a

Prostate-specific antigen or digital rectal exam.

Statistical analyses were performed in SAS version 9.2. We assessed statistically significant (two-sided, p<0.05) differences between diabetics and non-diabetics for potential confounders using chi-square tests. We used unconditional logistic regression to estimate the odds ratios (OR) and 95% CIs for prostate cancer screening associated with diabetes. Interaction terms, the product of diabetes and the putative effect modifiers (age, maximum BMI, marital status and health insurance), were added to logistic regression models and likelihood ratio tests were performed to test for effect modification.

Results

Table 1 presents characteristics of black men who were (n=4,283, 23.8%) and were not (n=13,695) screened for prostate cancer in the past 12 months. Compared to men who were not screened, black men who were screened were significantly older, had a higher household income and educational level, and were more likely to be married or living with a partner, have private insurance, have a higher maximum BMI, have hypertension, be taking cholesterol medications, and be never or former smokers. Similar patterns were seen when comparing screened (n=1,913, 31.3%) and unscreened (n=4,201) white men.

Table 2 presents the association between diabetes measures and prostate cancer screening within the past 12 months by race, adjusted for all variables except smoking whose addition to the model did not materially change OR estimates. Overall, 22.1% of non-diabetic black men and 33.1% of diabetic black men had been screened for prostate cancer. Prostate cancer screening was modestly but significantly more prevalent among men with versus without diabetes (OR 1.12, 95% CI 1.01-1.25). Utilizing <1 year between diabetes diagnosis and prostate cancer screening as the reference, prostate cancer screening among diabetics was greatest in the first year after diabetes diagnosis, after which no excess was observed and screening remained fairly stable with time. There was no significant effect of year of diabetes diagnosis or use of diabetes medications on prostate cancer screening.

Table 2. Odds ratios of prostate cancer screening within the past 12 months associated with diabetes measures by race, Southern Community Cohort Study, 2002-2009.

Screeneda Not screened

Characteristic n % n % ORc 95% CId

Black Men
Self-reported diabetes
 No 3327 77.7 11761 85.9 1.0 Referent
 Yes 956 22.3 1934 14.1 1.12 1.01-1.25
Time since diabetes diagnosis (years)b
 <1 86 9.2 158 8.3 1.0 Referent
 1-4 291 31.1 599 31.5 0.74 0.53-1.02
 5-9 227 24.3 475 25.0 0.69 0.49-0.96
 10-14 150 16.0 302 15.9 0.64 0.45-0.92
 15-19 82 8.8 145 7.6 0.71 0.47-1.08
 ≥20 100 10.7 223 11.7 0.51 0.35-0.76
Year of diabetes diagnosisb
 Pre-1994 290 31.0 571 30.0 1.0 Referent
 Post-1994 646 69.0 1331 70.0 1.11 0.92-1.35
Diabetes medicationsb
 No 134 14.1 310 16.1 1.0 Referent
 Yes 819 85.9 1621 83.9 1.06 0.83-1.36

White Men

Self-reported diabetes
 No 1559 81.5 3666 87.3 1.0 Referent
 Yes 354 18.5 535 12.7 1.25 1.03-1.51
Time since diabetes diagnosis (years)b
 <1 41 11.8 54 10.2 1.0 Referent
 1-4 112 32.2 186 35.2 0.65 0.36-1.16
 5-9 91 26.2 137 25.9 0.71 0.39-1.29
 10-14 44 12.6 77 14.6 0.59 0.30-1.16
 15-19 24 6.9 27 5.1 0.74 0.32-1.69
 ≥20 36 10.3 48 9.1 0.76 0.37-1.57
Year of diabetes diagnosisb
 Pre-1994 85 24.4 116 21.9 1.0 Referent
 Post-1994 263 75.6 413 78.1 0.86 0.59-1.26
Diabetes medicationsb
 No 71 20.1 116 21.7 1.0 Referent
 Yes 282 79.9 419 78.3 1.18 0.79-1.78
a

Prostate-specific antigen or digital rectal exam.

b

Among diabetics.

c

Odds ratio adjusted for age, annual household income, educational level, marital status, health insurance coverage, recruitment source, BMI at age 21 years and maximum, hypertension, cholesterol medications, and leisure-time moderate and vigorous physical activity during their 30s as categorized in Table 1.

d

95% Confidence interval.

Among white men, 29.8% of non-diabetics and 39.8% of diabetics had been screened for prostate cancer. Diabetes was significantly associated with increased odds of prostate cancer screening (OR 1.25, 95% CI 1.03-1.51). Among those with diabetes, we did not observe statistically significant differences according to time since diabetes diagnosis, but similar to the pattern in blacks, there appeared to be an excess of screening in the first year after diabetes diagnosis, after which the prostate cancer screening rate remained stable. Again, similar to black men, there was no effect of year of diabetes diagnosis or use of diabetes medications on prostate cancer screening. Age, maximum BMI, marital status and health insurance did not significantly modify the association between diabetes and prostate cancer screening among blacks or whites (not shown).

We performed a sensitivity analysis among diabetic men only who had been screened for prostate cancer (not shown). Time between diabetes diagnosis and recent prostate cancer screening was categorized as <1 year, 1-2 years, 3-5 years, 6-9 years and 10 or more years. Among diabetic men who were screened for prostate cancer, white men were significantly more likely than black men to have been screened within one year of diagnosis (14.7% vs. 11.6%, p=0.04). In contrast, black men were significantly more likely than white men to have been screened 10 or more years after their diagnosis (34.0% vs. 26.4%, p=0.001).

Discussion

Research on the role of prostate cancer screening in the association between diabetes and prostate cancer risk raised the possibility of a variable effect depending upon timing of the screening. A meta-analysis [3] found a more pronounced inverse association between diabetes and prostate cancer risk for studies conducted after 1994 (RR 0.73, 95% CI 0.64-0.83), when PSA screening became widespread, than those conducted before 1994 (RR 0.94, 95% CI 0.85-1.03). However, a case-control study of black and white men conducted after initiation of widespread PSA testing found no difference in the reduction of prostate cancer risk associated with diabetes among those men who reported they received annual prostate cancer screening (OR 0.68, 95% CI 0.41-1.12) compared to those screened less frequently (OR 0.61, 95% CI 0.36-1.01) [12].

In contrast with studies of diabetes and breast cancer screening which reported negative associations [13-16], we found that diabetes is modestly but significantly associated with increased likelihood of having a recent prostate cancer screening test among black and white men. However, the influence of diabetes on screening practices appeared largely restricted to the first year after a diabetes diagnosis, with similarly elevated OR estimates for screening during the first year among black and white men, albeit statistically significant only among black men. The associations between diabetes and breast and prostate cancer also differ, with greater likelihood of postmenopausal breast cancer associated with diabetes [17-20] and less likelihood of prostate cancer associated with diabetes [21].

Healthcare access, insurance coverage, and other socio-economic characteristics, as well as race, are all associated with PSA testing practices and cancer stage at detection. In our study population of black and white men with similarly low socioeconomic status (SES) and similar access to care, a positive association between diabetes and prostate cancer screening may be expected. Additionally, past prostate cancer screening recommendations [22-24], are consistent in suggesting increased prostate cancer screening for black men, who are at higher risk of prostate cancer compared with white men. Thus, primary care physicians face the challenge of not only considering the patient's age and race, but also overall health and co-morbidity status, in guiding the patient to an informed judgment as to the benefits of screening. Additionally, diabetes has been linked to increased risk of benign prostatic hyperplasia [25], suggesting the possibility that diabetes patients experiencing lower urinary tract symptoms should be preferentially screened at diagnosis to remove prostate cancer as a differential diagnosis. Furthermore, obesity is more prevalent among diabetes patients and thus may contribute to lower blood PSA levels [26-28], increasing the need for more frequent screening; however, we controlled for BMI in our analyses.

Preferential screening of men with diabetes may impact the interpretation of epidemiologic findings [1, 2] that prostate cancer risk initially increased following a diabetes diagnosis, before decreasing with extended follow-up. Thus, the long-term decreased risk of prostate cancer may result in part from enhanced detection near the time of diabetes diagnosis, as the lead time induced by active screening and removal of latent prostate cancers early during the follow-up period may remove prostate cancers that would have been diagnosed during extended follow-up. Future cohort investigations of diabetes and prostate cancer should consider collecting detailed data on PSA screening history to control for time varying effects of prostate cancer detection. Indeed, interpretation of past prostate cancer analyses have been altered with adjustment for prostate cancer screening [29].

Our study relied on self-reports of diabetes and prostate cancer screening which may have been affected by faulty memory or low literacy, or misclassification due to undiagnosed diabetes or inaccurate reports of timing of prostate cancer screening. However, the majority of SCCS participants were patients at CHCs, which provide primary healthcare to the underserved, and a validation sub-study found over 95% of self-reported diabetes in the SCCS could be confirmed through medical chart review [9]. It is possible that initiation of prostate cancer screening preceded or occurred simultaneously with a diabetes diagnosis in a subset of the baseline cohort, however we analyzed prostate cancer screening in the 12 months prior to cohort entry so that diabetes preceded prostate cancer screening for the vast number of study participants reporting a diabetes diagnosis. While we adjusted for health care coverage as a dimension of health care access, we were unable to adjust for usual source of care.

Study strengths include the large size of the population allowing for investigation of associations in black and white men separately. Confounding by socioeconomic factors is likely to be minimal, because blacks and whites were of similar SES upon recruitment and residual differences in education and income were accounted for in the statistical analyses. We adjusted for a wide range of confounders including obesity, hypertension, and cholesterol medication use, as well as health insurance coverage to isolate the effect of diabetes on prostate cancer screening apart from its effect on access to care.

In conclusion, diabetes was positively associated with prostate cancer screening especially during the short term following a diabetes diagnosis. Although racial differences in healthcare recommendations have been described by the Institute of Medicine [30], we found similar results for prostate cancer screening by diabetes status among black and white men. The early increase in prostate cancer detection, followed by lower prostate cancer detection over time, may partially explain the overall reduction in prostate cancer risk associated with diabetes.

Acknowledgments

The Southern Community Cohort Study was supported by the National Cancer Institute (NCI; grant R01 CA92447). Maureen Sanderson, Jay Fowke and Flora Ukoli received partial funding from the Department of Defense (DOD; grant W81XWH 11 PCRP STPA). Margaret K. Hargreaves received partial funding from the National Institutes of Health (NIH; grants 5P60 DK20593-24 and 5U01 CA114641-05). The authors would like to thank Jacquelyn S. Favours for her work on the manuscript.

Footnotes

Conflict of Interest: The authors declare that they have no conflict of interest.

References

  • 1.Rodriguez C, Patel AV, Mondul AM, Jacobs EJ, Thun MJ, Calle EE. Diabetes and risk of prostate cancer in a prospective cohort of US men. Am J Epidemiol. 2009;161:147–152. doi: 10.1093/aje/kwh334. [DOI] [PubMed] [Google Scholar]
  • 2.Kasper JS, Liu Y, Giovannucci E. Diabetes mellitus and risk of prostate cancer in the Health Professionals Follow-up Study. Int J Cancer. 2009;124:1398–1403. doi: 10.1002/ijc.24044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Kasper JS, Giovannucci E. A meta-analysis of diabetes mellitus and the risk of prostate cancer. Cancer Epidemiol Biomarkers Prev. 2006;15:2056–2062. doi: 10.1158/1055-9965.EPI-06-0410. [DOI] [PubMed] [Google Scholar]
  • 4.Kasper JS, Liu Y, Pollak MN, Rifai N, Giovannucci E. Hormonal profile of diabetic men and the potential link to prostate cancer. Cancer Causes Control. 2008;19:703–710. doi: 10.1007/s10552-008-9133-x. [DOI] [PubMed] [Google Scholar]
  • 5.Wright JL, Stanford JL. Metformin use and prostate cancer in Caucasian men: results from a population-based case-control study. Cancer Causes Control. 2009;20:1617–1622. doi: 10.1007/s10552-009-9407-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Willett WC. Diabetes mellitus and risk of prostate cancer (United States) Cancer Causes Control. 1998;9:3–9. doi: 10.1023/a:1008822917449. [DOI] [PubMed] [Google Scholar]
  • 7.Waters KM, Henderson BE, Stram DO, Wan P, Kolonel LN, Haiman CA. Association of diabetes with prostate cancer risk in the Multiethnic Cohort. Am J Epidemiol. 2009;69:937–945. doi: 10.1093/aje/kwp003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Atchison EA, Gridley G, Carreon JD, Leitzmann MF, McGlynn KA. Risk of cancer in a large cohort of U.S. veterans with diabetes. Int J Cancer. 2011;128:635–643. doi: 10.1002/ijc.25362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Signorello LB, Hargreaves MK, Blot WJ. The Southern Community Cohort Study: investigating health disparities. J Health Care Poor Underserved. 2010;21:26–37. doi: 10.1353/hpu.0.0245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Fowke JH, Motley SS, Barocas DA, Cookson MS, Concepcion R, Byerly S, et al. The associations between statin use and prostate cancer screening, prostate size, high-grade prostatic intraepithelial neoplasia (PIN), and prostate cancer. Cancer Causes Control. 2011;22:417–426. doi: 10.1007/s10552-010-9713-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Fowke JH, Schlundt D, Signorello LB, Ukoli FA, Blot WJ. Prostate cancer screening between low-income African-American and Caucasian men. Urol Oncol. 2205;23:333–340. doi: 10.1016/j.urolonc.2005.01.002. [DOI] [PubMed] [Google Scholar]
  • 12.Coker AL, Sanderson M, Zheng W, Fadden MK. Diabetes mellitus and prostate cancer risk among older men: a population-based study. Br J Cancer. 2004;90:2171–2175. doi: 10.1038/sj.bjc.6601857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Fontana SA, Baumann LC, Helberg C, Love RR. The delivery of preventive services in primary care practices according to chronic disease status. Am J Public Health. 1997;87:1190–1196. doi: 10.2105/ajph.87.7.1190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Beckman TJ, Cuddihy RM, Scheitel SM, Naessens JM, Killian JM, Pankratz VS. Screening mammogram utilization in women with diabetes. Diabetes Care. 2001;24:2049–2053. doi: 10.2337/diacare.24.12.2049. [DOI] [PubMed] [Google Scholar]
  • 15.McBean AM, Yu X. The underuse of screening services among elderly women with diabetes. Diabetes Care. 2007;30:1466–1472. doi: 10.2337/dc06-2233. [DOI] [PubMed] [Google Scholar]
  • 16.Lipscombe LL, Hux JE, Booth GL. Reduced screening mammography among women with diabetes. Arch Intern Med. 2005;165:2090–2095. doi: 10.1001/archinte.165.18.2090. [DOI] [PubMed] [Google Scholar]
  • 17.Wolf I, Sadetzki S, Catane R, Karasik A, Kaufman B. Diabetes mellitus and breast cancer. Lancet Oncol. 2005:103–111. doi: 10.1016/S1470-2045(05)01736-5. [DOI] [PubMed] [Google Scholar]
  • 18.Larsson SC, Mantzoros CS, Wolk A. Diabetes mellitus and risk of breast cancer: a meta-analysis. Int J Cancer. 2007;121:856–862. doi: 10.1002/ijc.22717. [DOI] [PubMed] [Google Scholar]
  • 19.Xue F, Michels K. Diabetes, metabolic syndrome, and breast cancer: a review of the current evidence. Am J Clin Nutr. 2007;86(suppl):832S–835S. doi: 10.1093/ajcn/86.3.823S. [DOI] [PubMed] [Google Scholar]
  • 20.Liao S, Li J, Wei W, Wang L, Zhang Y, Li J, Wang C, Sun S. Association between diabetes mellitus and breast cancer risk: a meta-analysis of the literature. Asian Pac J Cancer Prev. 2011;12:1061–1065. [PubMed] [Google Scholar]
  • 21.Kasper JS, Giovannucci E. A meta-analysis of diabetes mellitus and the risk of prostate cancer. Cancer Epidemiol Biomarkers Prev. 2006;15:2056–2062. doi: 10.1158/1055-9965.EPI-06-0410. [DOI] [PubMed] [Google Scholar]
  • 22.American Cancer Society. Cancer Facts & Figures 2012. American Cancer Society; Atlanta: 2012. [Google Scholar]
  • 23.American Urological Association. Prostate-specific antigen: best practice statement 2009 update. American Urological Association; Baltimore: 2009. [Google Scholar]
  • 24.US Preventive Services Task Force. Screening for prostate cancer. U.S. Preventive Services Task Force; Washington, DC: 2012. [Google Scholar]
  • 25.Parsons JK, Carter HB, Partin AW, Windham BG, Metter EJ, Ferrucci L, et al. Metabolic factors associated with benign prostatic hyperplasia. J Clin Endocrinol Metab. 2006;91:2562–2568. doi: 10.1210/jc.2005-2799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Muller H, Raum E, Rothenbacher D, Stegmaier C, Brenner H. Association of diabetes and body mass index with levels of prostate-specific antigen cutoff values? Cancer Epidemiol Biomarkers Prev. 2009;18:1350–1356. doi: 10.1158/1055-9965.EPI-08-0794. [DOI] [PubMed] [Google Scholar]
  • 27.Fowke JH, Matthews CM, Buchowski MS, Signorello LB, Chang SS, Cookson MS, et al. Association between prostate-specific antigen and leptin, adiponectin, HbA1c or C-peptide among Black and White men. Prostate Cancer Prostatic Dis. 2008;11:264–269. doi: 10.1038/sj.pcan.4501022. [DOI] [PubMed] [Google Scholar]
  • 28.Fowke JH, Matthews CE. PSA and body composition by dual X-ray absorptiometry (DXA) in NHANES. Prostate. 2010;70:120–125. doi: 10.1002/pros.21039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Porter MP, Stanford JL. Obesity and the risk of prostate cancer. The Prostate. 2005;62:316–321. doi: 10.1002/pros.20121. [DOI] [PubMed] [Google Scholar]
  • 30.Institute of Medicine. Unequal treatment: confronting racial and ethnic disparities in health care. Institute of Medicine; Washington, DC: 2003. [Google Scholar]

RESOURCES