Introduction
Digital Rectal Exam (DRE) is a medical procedure where a lubricated gloved finger is inserted into the rectum to check for abnormalities, enlargements, lumps, tenderness, and hardness in the prostate, rectum, and pelvis.1 Since the DRE only reaches the back wall of the prostate glands, the anomaly of the front and middle parts of the prostate gland cannot be ascertained. As these areas of the prostate are not accessible from outside the body, the utility of a single DRE has been questioned in screening for prostate cancer, as it is considered less reliable than Prostate Specific Antigen (PSA) blood test.1–3 A meta-analysis of 8 studies with 85,798 participants showed that the positive predictive value (PPV) of DRE and PSA are approximately the same: 0.21 (95% CI = 0.13–0.33) and 0.22 (95% CI = 0.15–0.30), respectively, with no additional benefit observed when combining DRE and PSA (PPV = 0.22, 95% CI = 0.13–0.26).4 This meta-analysis concluded that the cancer detection rate was lower for DRE than PSA.
Since early-stage prostate cancer is typically asymptomatic, both DRE and PSA tests are used for screening. The existing guidelines for DRE screening were developed in conjunction with PSA testing through randomized trials to enhance biopsy decision-making. For instance, the US Preventive Services Task Force (USPSTF) recommends biennial DRE in conjunction with PSA testing for men with hypogonadism and for those with PSA less than 2.5 ng/mL.5,6 The National Comprehensive Cancer Network (NCCN) recommends a prostate biopsy if the PSA value exceeds 3.0 ng/mL or if the DRE result is very suspicious.7 The American Urological Association (AUA) advises that clinicians should consider performing DRE on patients with PSA levels of 2 ng/mL or higher to assess the risk of clinically significant cancer.8 However, the USPSTF does not recommend DRE as a standalone screening for prostate cancer despite cases where DRE has found prostate cancers in men with normal PSA levels.5 In contrast to the USPSTF, the German Statutory Early Detection Program has recommended stand-alone DRE for prostate cancer screening on 45+ years old male since 1971.9 DRE is also a part of clinical assessment tools such as European Randomized Study of Screening for Prostate Cancer.10 However, a multicentric randomized trial enrolling more than 46,000 men aged 45 years old to test for risk-adapted PSA screening for prostate cancer found that the stand-alone DRE screening for prostate cancer is poor because it also does not improve the detection of PSA-screen-detected prostate cancer and may not be recommended as a screening test for younger men.9 According to this randomized trial, out of 57 men with a suspicious DRE at the age of 45 years old, only 3 had actual prostate cancers. The calculated DRE detection rate was 0.05% (3/6537) compared with the 4x higher detection by 0.21% PSA screening (48/23301).9 The current study utilized trend analysis to detect abnormal DRE patterns, providing insights that may decrease the chance of false positives.
A meta-analysis of seven studies with 9,241 patients estimated the pooled sensitivity, specificity, and PPV of DRE to be 51%, 59%, and 41%, respectively.11 This meta-analysis recommends against routine DRE screening in the primary care setting. However, the majority of primary care physicians in Canada are routinely using DRE in the primary care setting and 38% of 955 physicians believe that DRE provides a survival benefit.12,13 In the United States, despite the impact of USPSTF guidelines on clinical practice, DRE is performed routinely by 84% of primary care physicians, particularly among men aged 50 and older.14 Until now, DRE remains to be an acceptable procedure as a standard of care in urology clinics.15
We presented numerous studies that have shown stand-alone DRE has poor performance in detecting prostate cancer in primary care settings. We hypothesize that long-term follow-up such as serial DRE testing in which repeated suspicious results might improve DRE detection rate.5,16 In this study, we utilized data from the Prostate, Lung, Colorectal, and Ovarian (PLCO) Cancer Screening Trial17 to evaluate whether long-term DRE screening offers crucial information for early detection of prostate cancer. This study examines 10-year trends of suspicious DRE findings among PLCO participants who were diagnosed or not diagnosed with prostate cancer. We theorize that the likelihood of suspicious DRE would change over time depending on prostate cancer status.
Materials and Methods
Study Population
A secondary analysis was conducted in the intervention arm from the PLCO Cancer Screening Trial.17 For this prospective study, participants aged 55–74 years were recruited from the US general population and randomly assigned to the intervention arm or the control arm at 10 clinical centers between November 1993 and July 2001.18 There was a nearly even split with 38,338 in the control arm that offered the standard care to participants and 38,340 in the intervention arm that underwent prostate cancer screening tests (total = 76,678). The PLCO trial was conducted in accordance with the Declaration of Helsinki. All participants were given informed consent, and the research was approved by the institutional review boards of all the 10 participating centers and the US National Cancer Institute (NCI). This study received approval (PLCO-1141) from the NCI to access deidentified data sets. PLCO trial design and methodology have been published previously.19
Study Inclusion and Exclusion
The PLCO Cancer Screening Trial includes participants who meet the eligibility criteria, and they receive either usual care as the control (N=38,338) or annual screening (N=38,340).19 The usual care arm was excluded from the analysis due to the lack of DRE screening19 and excluded missing race (N=914). Due to the small sample sizes of some ethnic groups, we restricted the study to black and white and excluded all other races. Therefore, our final analytic file contains 34,756 male participants.
Measurements
DRE Measurement
Participants in the screening arm were screened annually using DRE at four visits. Thus, there were four DRE exams (T0–T3) before and at diagnosis among the 34,756 participants who completed at least one of the screenings. To maintain quality assurance, a sample of men were selected for a second DRE by an independent examiner during the same screening session. In cases of discordant results, personalized screening outcomes and diagnostic paths were assigned for each patient.19 Participants with a suspicious DRE were advised to seek diagnostic follow-up care from their primary care providers.18 The DRE findings ranged from 1 (negative), 2 (abnormal, suspicious), 3 (abnormal, non-suspicious), 4 (inadequate screen), 8 (not done, expected), and 9 (not done, not expected). The DRE findings for this study were classified into: 0 (normal), 1 (abnormal non-suspicious), and 2 (abnormal suspicious). DRE codes 4, 8, and 9 were treated as missing. We analyzed the DRE findings over a 10-year period before and at the prostate cancer diagnosis (positive/negative). The 10-year follow-up adequately demonstrates changes in DRE findings, as men who underwent DRE within 10 years of diagnosis experienced a significant reduction of prostate cancer-specific mortality.20 We defined the time at DRE result as the years before a positive or negative prostate cancer diagnosis (+ or -), where “0” represents the DRE result at the time of diagnosis (+ or -), and “-10” represents the DRE result “10” years prior to the diagnosis (+ or -). This calculation was based on days from randomization until the DRE test at each visit and days from randomization to a positive (+) or negative (-) prostate cancer.
Covariates
We included baseline data, such as participant age at randomization, body mass index (BMI) defined as weight (kg) divided by height (m2), education level (college degree: no, yes), race (Black, White), marital status (married: no, yes), frequent urination (defined as urinating three or more times a night: no, yes), immediate family history of prostate cancer (no, yes), and enlarged prostate or benign prostatic hypertrophy (BPH) (no, yes). The PLCO screening trial confirmed prostate cancer diagnoses via medical record abstraction such as a self-report of prostate cancer, death certificate indicating prostate cancer, and relative information to the screening center of the participant’s cancer. The assessment includes the question “does the participant have confirmed primary invasive prostate cancer diagnosed during the trial?”: 0 = “no confirmed prostate cancer” and 1 = “confirmed prostate cancer”.
Statistical Analyses
All data analyses were executed in SAS version 9.4 (SAS Institute Inc, Cary NC, United States). Numerical variables (age at randomization and baseline BMI) were presented as mean ± standard deviation (SD) and non-numerical variables (eg, race and education) were presented as count and percentage (Table 1). Proportions of normal, abnormal non-suspicious DRE, and abnormal suspicious DRE were compared across the sample characteristics using the Chi-square test (Tables 2–5). ANOVA test was used to compare age at randomization and baseline BMI across DRE findings (Tables 2–5). We modeled DRE results over a 10-year follow-up as binary outcomes: abnormal non-suspicious DRE vs normal DRE and abnormal suspicious DRE vs normal DRE. The trend in log odds ratio of abnormal DRE findings was modeled using repeated binary logistic regression via generalized estimating equation (GEE) with the exchangeable regression structure (LOGOR = EXCH). We examined the interaction effect, defined as the combination of follow-up year to diagnosis and prostate cancer status (+ or -) on the likelihood of having an abnormal non-suspicious DRE and an abnormal suspicious DRE, using normal DRE as the reference category. The model adjusted for age, education, marital status, baseline BMI, frequent urinating, family history, and BPH (Table 6). The results were presented in terms of adjusted odds ratio (aOR) and confidence intervals (CIs). CIs inclusive of 1.0 were considered non-significant association, while those without 1 were considered significant association. P-value (P) of less than or equal to 0.05 was considered statistically significant.
|
Table 1 Sample Characteristics (N = 34,756 Participants)
|
 |
Table 2 Assessing the Association Between DRE Findings and Sample Characteristics at the Baseline Visit (T0) (N= 34,756 Participants)
|
 |
Table 3 Assessing the Association Between DRE Findings and Sample Characteristics at the First Visit (T1) (N= 34,756 Participants)
|
 |
Table 4 Assessing the Association Between DRE Findings and Sample Characteristics at the second Visit (T2) (N= 34,756 Participants)
|
 |
Table 5 Assessing the Association Between DRE Findings and Sample Characteristics at the Third Visit (T3) (N= 34,756 Participants)
|
 |
Table 6 GEE Analysis of Adjusted Odds Ratio of Abnormal DRE as Compared to Normal DRE
|
Results
Table 1 describes the characteristics of a subsample from the PLCO intervention arm (N=34,756). Of these, 12.3% (4280/34756) had prostate cancer with significantly higher estimates in Black men than in White men (15.1% vs 12.2%, P < 0.001). At the end of the follow-up, the percentage of abnormal suspicious DRE was significantly increased from 6.5% at 10 years prior to diagnosis to 27.2% at diagnosis.
The frequency distribution of normal, abnormal non-suspicious, and abnormal suspicious DRE by the sample characteristics at the baseline visit (T0), visit 1 (T1), visit 2 (T2), and visit 3 (T3) are displayed in Tables 2–5, respectively. In this subgroup analysis, we observed significant association between DRE findings and race, education, and BPH at all four visits. For instance, the percentage of abnormal DRE was lower among Black participants than White participants at all four visits. Age at randomization and baseline BMI were significantly different across DRE findings at all four visits. Specifically, age was positively associated with abnormal DRE findings, while baseline BMI was inversely associated with abnormal DRE findings.
Table 6 presents the results of the GEE analysis of the changes in DRE findings across time (follow-up years to diagnosis) by prostate cancer status. The interaction term (follow-up year to diagnosis × prostate cancer status) was statistically significant, indicating that the likelihood of abnormal DRE findings changes significantly over time between prostate cancer and non-prostate cancer participants. Each year closer to diagnosis, the prostate cancer participants were expected to increase the odds of abnormal non-suspicious DRE by 5.2% (aOR=1.052, 95% CI: 1.033–1.072) and abnormal suspicious DRE by 23.0% (aOR=1.230, 95% CI: 1.193–1.268). The probability of abnormal suspicious DRE increases sharply over time in participants with prostate cancer (Figure 1), while the probability of abnormal non-suspicious DRE increases gradually over time in participants with prostate cancer (Figure 2). There is no change in DRE overtime in participants who did not have prostate cancer.
 |
Figure 1 Predicted probability of an abnormal suspicious DRE by follow-up year to diagnosis and prostate cancer status. The probability of having an abnormal suspicious DRE goes up with prostate cancer vs no prostate cancer. Changes in trend observed 8 years before a positive or negative prostate cancer result.
|
 |
Figure 2 Predicted probability of an abnormal non-suspicious DRE by follow-up year to diagnosis and prostate cancer status.
|
Older age is associated with higher odds of abnormal DRE, where the odds of abnormal non-suspicious DRE tend to increase by 1.0% for every year increase in age (aOR=1.010, 95% CI: 1.006–1.014) and the odds of abnormal suspicious DRE tend to increase by 4.8% for every year increase in age (aOR=1.048, 95% CI: 1.040–1.055) (Table 6). The odds of abnormal non-suspicious DRE (aOR=0.803, 95% CI: 0.724–0.892) and abnormal suspicious DRE (aOR=0.735, 95% CI: 0.611–0.883) were significantly lower in Black participants compared to White participants. PLCO participants with a college degree had 8.5% lower odds of abnormal non-suspicious DRE (aOR=0.915, 95% CI: 0.874–0.958) and 17.6% lower odds of abnormal suspicious DRE (aOR=0.824, 95% CI: 0.761–0.893) when compared with PLCO participants without a college degree. Participants with higher BMI had lower odds of abnormal DRE, where the odds of abnormal non-suspicious DRE tend to decrease by 1.2% for every kg/m2 increase in BMI (aOR=0.988, 95% CI: 0.983–0.994) and the odds of abnormal suspicious DRE tend to decrease by 2.4% for every kg/m2 increase in BMI (aOR=0.976, 95% CI: 0.967–0.986). BPH associated with increased odds of abnormal non-suspicious DRE by 57.9% (aOR=1.571, 95% CI: 1.491–1.672) and increased odds of abnormal suspicious DRE by 68.9% (aOR=1.689, 95% CI: 1.541–1.852). Frequent urination and immediate family history of prostate cancer did not affect the odds risk of having abnormal DRE findings (Table 6).
Discussion
This study utilized secondary analysis of follow-up data on 34,756 men from the PLCO Screening Trial to explore changes in the likelihood of abnormal suspicious DRE by investigating the interaction term follow-up year to diagnosis × prostate cancer status. The overall crude prevalence of abnormal suspicious DRE increased over time from 6.5% at 10 years prior to diagnosis to 27.2% at diagnosis. Our GEE model provides evidence to support the research hypothesis by identifying an increasing trend in the likelihood of abnormal suspicious DRE (Figure 1) and abnormal non-suspicious DRE (Figure 2) among men with prostate cancer compared to men without prostate cancer.
We propose that there is still utility in performing DREs consistent with USPTF and AUA as we addressed an important gap in developing a model for long-term follow-up of DRE screening to reduce potential harms associated with a single DRE test.5,6 Unlike studies that considered DRE as a one-time screening,9 our study endorses the usage of long-term follow-up of DRE in primary care settings. A one-time DRE screening is not an effective approach as it misses true positive cases. For instance, Krilaviciute et al reported low detection for prostate cancer of 0.05%, while our study detection rate increases over time: 0.64% at 10 years prior to diagnosis, 6.32% at 5 years prior to diagnosis, 12.60% at 2 years prior to diagnosis, and 43.4% at diagnosis. The positive predictive value of abnormal suspicious DRE was 4.74% at 10 years prior to diagnosis, 36.82% at 5 years prior to diagnosis, 60.63% at 2 years prior to diagnosis, and 90.48% at diagnosis. This is similar to a previous study that reported a high chance of developing prostate cancer in men with suspicious DRE tests at the initial screening, second screening, and third screening.21 This suggests that the long-term follow-up of DRE screening is an important and a reliable approach in detecting prostate cancer.
Our study identified several other key factors influencing the likelihood of abnormal suspicious DRE. Black men had significantly lower likelihood of abnormal DRE than White men. The reasons for this difference are not fully understood, but it might be explained by the psychological fear regarding DRE impacting the screening practices and the likelihood of being screened across different race groups as Black men undergo DRE less often and have higher DRE screening fears than White men.1,22 The DRE screenings rate was much lower for Black men as compared to White men due to the lack of recruitment of Black men.23
Our findings reveal a low BMI value is an indicator of abnormal DRE findings as we found an inverse correlation between baseline BMI and abnormal DRE. Studies suggest that obese men were less likely to have abnormal DRE findings24 and less likely to have abnormal prostate cancer.25 DRE in obese men presents unique considerations due to the increased tissue in the pelvic area. This may require skilled examiners to physically evaluate the prostate gland for presence of any abnormalities or loss of anatomic landmarks. Therefore, careful DREs in obese patients are vital to ensure effective DRE screening.
Our study showed that men with BPH were associated with greater odds of abnormal DRE than men without BPH. This finding has not been extensively explored, but a study found that abnormal DRE was an independent factor of incidental prostate cancer following BPH surgery.26 We suggest that BPH nodules can mimic nodules caused by prostate cancer on DRE, which has also been shown on prostate MRIs. The current study suggests that older men were more likely to have abnormal DRE findings. Age significantly correlated with prostate cancer.25 Older age may affect the structure of the prostate and can be interpreted as abnormal, which may contribute to false positive results.
Notwithstanding, our study comes with limitations secondary to the inherent nature of retrospective analysis. The study findings may not be generalizable to the African American population due to the greater representations of one race over another may have affected our results23 as there are more white participants than black participants in the PLCO trial. Unlike the DRE, which has multiple assessments (T0–T3), the prostate cancer status was determined according to one assessment via medical record abstraction such as a self-report of prostate cancer, death certificates indicating prostate cancer, and relative informing the screening center of the participant’s prostate cancer status. Inadequate DRE screening and not completed exams were treated as missing. Consequently, the authors were unable to use GEE analysis to assess the trends of prostate cancer changes within a period of 10 years prior to diagnosis.
The current study, however, has several strengths 1) the PLCO trial is a population-based study and serial DRE testing might represent the study populations, 2) the definition of DRE classification was clearly defined and reproducible to limit interpretation errors amongst clinicians performing DREs, 3) we show the importance of serial DREs overtime in raising the clinical suspicion of prostate cancer as well as its status as an important, feasible, and cost-effective adjunct to serum PSA screening in prostate cancer, and 4) our analysis has been adjusted for age at randomization, BMI, education level, race, marital status, frequent urination, immediate family history, and BPH.
Conclusion
Our results suggest that incorporating serial DRE findings into screening strategies may reduce false positives and improve early detection of clinically significant prostate cancer. This study demonstrates a rising probability of abnormal DRE findings in men with prostate cancer, whereas no temporal change was observed in men without prostate cancer. Long-term follow-up DRE findings can help identify the changes in the prostate gland due to aging to reduce the false positives associated with the PSA test.
Data Sharing Statement
Requests to access the PLCO datasets should be directed to the National Cancer Institute (NCI) Cancer Data Access System (CDAS): https://cdas.cancer.gov/plco/.
Ethics Statement
The PLCO study was approved by the Institutional Review Boards of participating centers and the NCI. The study participants provided written informed consent. Ethical approval was not required. The authors analyzed secondary data from the Prostate, Lung, Colorectal, and Ovarian cancer screening trial.
Acknowledgments
We acknowledge the study participants for their contributions to making this study possible. The authors thank the National Cancer Institute for providing access to data.
The contents of this publication are the sole responsibility of the author(s) and do not necessarily reflect the views, opinions or policies of Uniformed Services University of the Health Sciences (USUHS), The Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., the Department of Defense (DoD), the Departments of the Army, Navy, or Air Force. Mention of trade names, commercial products, or organizations does not imply endorsement by the US Government.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Author Contributions
All authors made a significant contribution to the work reported, whether that is in the conception, study design, execution, acquisition of data, analysis and interpretation, or in all these areas; took part in drafting, revising or critically reviewing the article; gave final approval of the version to be published; have agreed on the journal to which the article has been submitted; and agree to be accountable for all aspects of the work.
Funding
There is no funding to report.
Disclosure
The authors declare no commercial or financial relationships that could be constructed as a potential conflict of interest for this work.
References
1. Kirby M, Merriel SW, Olajide O, et al. Is the digital rectal exam any good as a prostate cancer screening test? Br J Gen Pract. 2024;74:137–139. doi:10.3399/bjgp24X736677
2. Shish L, Zabell J. Digital rectal exam in prostate cancer screening and elevated PSA work-up-is there a role anymore? Curr Urol Rep. 2024;25:193–199. doi:10.1007/s11934-024-01218-4
3. Bouras S. Digital rectal exam in prostate cancer screening: a critical review of the ERSPC Rotterdam study. Afr J Urol. 2024;30:51. doi:10.1186/s12301-024-00449-8
4. Matsukawa A, Yanagisawa T, Bekku K, et al. Comparing the performance of digital rectal examination and prostate-specific antigen as a screening test for prostate cancer: a systematic review and meta-analysis. Eur Urol Oncol. 2024;7:697–704. doi:10.1016/j.euo.2023.12.005
5. Force USPST. Screening for Prostate Cancer: US Preventive Services Task Force Recommendation Statement. JAMA. 2018;319:1901–1913. doi:10.1001/jama.2018.3710
6. US Preventive Services Task Force. Screening for Prostate Cancer: U.S. Preventive Services Task Force Recommendation Statement. Ann Internal Med. 2008;149(3):185–191. doi:10.7326/0003-4819-149-3-200808050-00008
7. Aghazadeh MA, Frankel J, Belanger M, et al. National Comprehensive Cancer Network® favorable intermediate risk prostate cancer-is active surveillance appropriate? J Urol. 2018;199:1196–1201. doi:10.1016/j.juro.2017.12.049
8. Wei JT, Barocas D, Carlsson S, et al. Early detection of prostate cancer: AUA/SUO guideline part II: considerations for a prostate biopsy. J Urol. 2023;210:54–63. doi:10.1097/JU.0000000000003492
9. Krilaviciute A, Becker N, Lakes J, et al. Digital rectal examination is not a useful screening test for prostate cancer. Eur Urol Oncol. 2023;6:566–573. doi:10.1016/j.euo.2023.09.008
10. Roobol MJ, Schröder FH, Hugosson J, et al. Importance of prostate volume in the European Randomised Study of Screening for Prostate Cancer (ERSPC) risk calculators: results from the prostate biopsy collaborative group. World J Urol. 2012;30:149–155. doi:10.1007/s00345-011-0804-y
11. Naji L, Randhawa H, Sohani Z, et al. Digital rectal examination for prostate cancer screening in primary care: a systematic review and meta-analysis. Ann Fam Med. 2018;16:149–154. doi:10.1370/afm.2205
12. Allard CB, Dason S, Lusis J, Kapoor A. Prostate cancer screening: attitudes and practices of family physicians in Ontario. Can Urol Assoc J. 2012;6:188–193. doi:10.5489/cuaj.11290
13. Akerman JP, Allard CB, Tajzler C, Kapoor A. Prostate cancer screening among family physicians in Ontario: an update on attitudes and current practice. Can Urol Assoc J. 2018;12:E53–e58. doi:10.5489/cuaj.4631
14. Fawzy A, Fontenot C, Guthrie R, Baudier MM. Practice patterns among primary care physicians in benign prostatic hyperplasia and prostate cancer. Fam Med. 1997;29:321–325.
15. Cui T, Kovell RC, Terlecki RP. Is it time to abandon the digital rectal examination? Lessons from the PLCO cancer screening trial and peer-reviewed literature. Curr Med Res Opin. 2016;32:1663–1669. doi:10.1080/03007995.2016.1198312
16. Martínez de Hurtado J, Chéchile Toniolo G, Villavicencio Mavrich H. [The digital rectal exam, prostate-specific antigen and transrectal echography in the diagnosis of prostatic cancer]. Arch Esp Urol. 1995;48:247–259. Danish
17. Gohagan JK, Prorok PC, Hayes RB, Kramer BS. The Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial of the National Cancer Institute: history, organization, and status. Control Clin Trials. 2000;21:251s–272s. doi:10.1016/S0197-2456(00)00097-0
18. Andriole GL, Levin DL, Crawford ED, et al. Prostate Cancer Screening in the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial: findings from the initial screening round of a randomized trial. J Natl Cancer Inst. 2005;97:433–438. doi:10.1093/jnci/dji065
19. Prorok PC, Andriole GL, Bresalier RS, et al. Design of the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial. Control Clin Trials. 2000;21:273s–309s. doi:10.1016/S0197-2456(00)00098-2
20. Thompson IM, Zeidman EJ. Presentation and clinical course of patients ultimately succumbing to carcinoma of the prostate. Scand J Urol Nephrol. 1991;25:111–114. doi:10.3109/00365599109024543
21. Gosselaar C, Roobol MJ, Roemeling S, Schröder FH. The role of the digital rectal examination in subsequent screening visits in the European randomized study of screening for prostate cancer (ERSPC), Rotterdam. Eur Urol. 2008;54:581–588. doi:10.1016/j.eururo.2008.03.104
22. Lee DJ, Consedine NS, Spencer BA. Barriers and facilitators to digital rectal examination screening among African-American and African-Caribbean men. Urology. 2011;77:891–898. doi:10.1016/j.urology.2010.11.056
23. Eckersberger E, Finkelstein J, Sadri H, et al. Screening for prostate cancer: a review of the ERSPC and PLCO Trials. Rev Urol. 2009;11:127–133.
24. Dell’Atti L. The role of the digital rectal examination as diagnostic test for prostate cancer detection in obese patients. J Buon. 2015;20:1601–1605.
25. Ahmed AE, Martin CB, Dahman B, Chesnut GT, Kern SQ. General Obesity and Prostate Cancer in Relation to Abdominal Obesity and Ethnic Groups: a US population-based cross-sectional study. Res Rep Urol. 2024;16:235–244. doi:10.2147/RRU.S489915
26. Wang Y, Li X, Yang H, Yin C, Wu Y, Chen X. Predictive factors of incidental prostate cancer in patients undergoing surgery for presumed benign prostatic hyperplasia: an updated systematic review and meta-analysis. Front Oncol. 2025;15:1561675. doi:10.3389/fonc.2025.1561675