Journal of the National Cancer Institute Advance Access originally published online on September 25, 2007
JNCI Journal of the National Cancer Institute 2007 99(19):1484-1489; doi:10.1093/jnci/djm153
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© The Author 2007. Published by Oxford University Press.
ARTICLES |
Needle Biopsies on Autopsy Prostates: Sensitivity of Cancer Detection Based on True Prevalence
Affiliations of authors: Departments of Urology (GPH, NBD, RFJ) and Pathology (VC, MJ, GT, GdlR), State University of New York Upstate Medical University, Syracuse, NY; Departments of Epidemiology and Biostatistics (AMS, AJV) and Urology (RK, HL), Memorial Sloan-Kettering Cancer Center, New York, NY; Onondaga County Medical Examiner, Syracuse, NY (MJ)
Correspondence to: Gabriel P. Haas, MD, Department of Urology, State University of New York Upstate Medical University, 750 East Adams Street, Syracuse, NY 13210 (e-mail: haasg{at}upstate.edu).
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ABSTRACT |
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Background: It is difficult to estimate the diagnostic accuracy of biopsy for prostate cancer because men with negative biopsy do not undergo radical prostatectomy and thus have no confirmation of biopsy findings.
Methods: We performed 18-core needle biopsies on autopsy prostates from 164 men who had no history of prostate cancer. Six-core biopsies were taken from each of the mid peripheral zone (MPZ), the lateral peripheral zone (LPZ), and the central zone (CZ). We tested associations between age and tumor characteristics and analyzed the sensitivity of biopsies at each site. All statistical tests were two-sided.
Results: Prostate cancer was present in 47 (29%) prostates. Of the 47 cancers detected, 20 were clinically significant according to histologic criteria. Tumor volume was associated with tumor grade (P = .012) and with age (P<.001). The biopsies from the CZ did not detect any cancer that was not present in biopsies of either the MPZ or LPZ. The sensitivity of the biopsies taken from the MPZ and LPZ together (53%, 95% confidence interval [CI] = 38% to 68%) was therefore the same as that of 18-core biopsies and was superior to that of biopsies of the MPZ alone (30%, 95% CI = 17% to 45%) (P = .003). The sensitivities of biopsies from the MPZ for clinically significant and insignificant cancer were 55% (95% CI = 32% to 77%) and 11% (95% CI = 2% to 29%), respectively, compared with 80% (95% CI = 56% to 94%) and 33% (95% CI = 17% to 54%) for those from the MPZ and LPZ combined.
Conclusions: The ability to detect prostate cancer was more related to the biopsy site than to the number of biopsy cores taken. The 12-core biopsies, six cores each from the MPZ and LPZ, were most likely to detect the majority of clinically significant cancers but also detected many insignificant cancers. When the six-core biopsies from the CZ were added, no increase in sensitivity was observed.
Prior knowledge The accuracy of detecting prostate cancer in prostate biopsies is difficult to determine because most men whose biopsies do not show cancer do not undergo radical prostatectomy to confirm the results. Study design Eighteen-core needle biopsies were performed on autopsy prostates of men who had not been diagnosed with prostate cancer, six cores each from the mid peripheral zone (MPZ), the lateral peripheral zone (LPZ), and the central zone. The sensitivity and specificity of detecting prostate cancer from the biopsies were analyzed, as were associations between age and tumor characteristics. Contributions Of the 164 prostates biopsied, prostate cancer was detected in 47, of which, according to histologic criteria, 20 were felt to be clinically significant. Tumor volume was associated with age and tumor grade. The sensitivity of the 12-core biopsies taken from the MPZ and LPZ was similar to that of all 18-core biopsies and was higher than that of the six-core biopsies from the MPZ. Implications The anatomic location of the biopsy was more important than the total number taken. Limitations The study sample size was relatively small. None of the men had a previous history of prostate cancer, and all died of causes unrelated to prostate cancer, so all of the prostate cancers detected in this study would have been considered clinically insignificant.
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The sensitivity of detecting prostate cancer has been enhanced by lowering the threshold of serum prostate-specific antigen (PSA) concentration that is used to recommend biopsy and by increasing the number of samples taken at biopsy. As a result, this disease is now detected earlier in its development, as shown by the downward pathologic stage migration of prostate cancer in radical prostatectomy specimens (1,2). However, small and well-differentiated cancers, which are designated as clinically insignificant (3,4), may not be of immediate threat and should not be managed with radical and possibly morbid treatment. Biopsy strategies should therefore be designed to detect the maximum number of clinically significant cancers and the minimum number of clinically insignificant lesions.
Many prostate cancers are latent, asymptomatic, and undetected through standard diagnostic tests (5). Studies evaluating prostate cancer detection are therefore influenced by verification bias (6). Indeed, the reference standard investigation, the prostate biopsy, is not performed on all patients because men with low serum PSA concentrations do not undergo biopsy and men whose prostate biopsy failed to detect cancer do not undergo surgical verification. Moreover, with the development of nonsurgical treatments, such as brachytherapy and external radiation therapy, not all patients have prostate specimens available for pathologic evaluation. Thus, the true sensitivity of various biopsy regimens is unknown.
The prevalence of prostate cancer has been evaluated by autopsy studies in several populations (7–10). These studies provide the opportunity to characterize the number, size, grade, and location of prostate cancer foci and could therefore be used to correct for the detection bias specific to clinical studies.
We investigated the ability of various biopsy regimens, which are characterized by the number and anatomic location of cores taken, to detect prostate cancer from autopsy prostates. The tumors were classified according to their size, grade, and location, and the sensitivity and specificity of the biopsy regimens were evaluated. Prostate cancer clinical significance was defined according to the criteria of Epstein et al. (3) and Stamey et al. (4). As commonly described, the term "clinically insignificant carcinoma" refers to biologically indolent disease that is not destined to metastasize or otherwise threaten the life or quality of life of the host (11).
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Subjects and Methods |
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Tissue Collection
We prospectively collected 202 consecutive prostate glands from deceased men that were provided by the University Hospital, Syracuse, NY; the Onondaga County Medical Examiner, Syracuse, NY; and the National Disease Research Interchange, Philadelphia, PA. Only age, race, and cause of death were recorded. This study used samples from decedents and was exempt from institutional review. The decedents had no known history of prostate cancer. At autopsy, the entire prostate gland, together with the seminal vesicles, was excised and placed in 10% neutral buffered formalin. In 38 (19%) samples, the entire prostate gland was not removed; these subjects were excluded, leaving 164 prostate glands available for analysis.
Prostate Biopsy
All biopsies were performed in a manner that mimicked clinical biopsy under the direction of a urologist (G. P. Haas) who has extensive experience with transrectal ultrasound-guided prostate biopsies. Biopsies were taken with a standard 18F spring-loaded biopsy gun (Bard Maxcore, C.R. Bard, Covengton, GA). The biopsy gun needle was inserted through the posterior surface of the hand-held gland, and bilateral samples were taken from the apex, mid gland, and base (Fig. 1). The first six cores, corresponding to the sextant biopsy protocol, were taken from the mid peripheral zone (MPZ). The next six cores were taken with the needle inserted into the central zone (CZ). The last six cores were taken from the lateral peripheral zone (LPZ). For each biopsy showing cancer, Gleason score, the number of tissue cores containing cancer, the percentage of cancer involvement in each core, and the location of the tumor in the gland were determined.
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Whole-Mount Prostate Processing and Histologic Evaluation
After the biopsies were taken, the glands were fixed in formalin for at least 72 hours. The glands were then separated from any surrounding tissue and weighed, and volumes were measured. Prostate volumes, which are not typically reported in clinical practice, were measured by water displacement. The glands were cut into 4-mm sections perpendicular to the posterior plane, labeled, embedded in paraffin, and further sectioned to produce 5-µm whole-mount sections that were stained with hematoxylin and eosin. A single pathologist (G. de la Roza) analyzed the biopsies and whole-mount slides in a blinded fashion. Each tumor focus detected was outlined. Suspicious diagnoses were confirmed with immunohistochemical analysis using basal cell markers p63 (Neomarkers, Freemont, CA) and P504S/alpha-methylacyl-CoA racemase (Biocare Medical, Concord, CA) (12). The total number of tumor foci and their locations were recorded. An area of carcinoma was considered to be a separate focus if it was separated from the nearest adjacent focus by a low-power field diameter (4.5 mm), as previously described (13). Each tumor focus was graded according to the modified Gleason grading system (14). Pathologic stage was determined according to the 2002 tumor–node–metastasis classification for prostate cancer (15).
Digital Reconstruction and Calculation of Tumor Volume
The surface of each tumor focus was determined by computerized planimetry using an image analysis program (ImageJ, National Institutes of Health, Bethesda, MD; http://rsb.info.nih.gov/ij/, 1997–2007) (16). Tumor volume was calculated by multiplying each tumor surface by the section thickness (4 mm) and by 1.5 to compensate for tissue shrinkage (17). The index tumor volume was defined as the volume of the largest focus of carcinoma. Total tumor volume was calculated as the sum of the volumes of the individual foci. Tumors were considered to be clinically insignificant if they were organ-confined with an index tumor volume of less than 0.5 cm3 and Gleason score 6 or less (3,4).
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Statistical Analysis |
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We distinguished different groups of tumors according to their pathologic features: index tumors of low (<0.5 cm3) versus high (
0.5 cm3) volume, low (
6) versus high (7) Gleason score, and unifocal (1 tumor focus) versus multifocal (>1 tumor focus) prostate cancers. These cut points were chosen according to the definition of clinically significant versus insignificant cancer (3,4). The association between these pathologic groupings and age was evaluated by logistic regression. McNemar's test was used to compare the sensitivity of cancer detection between 6-, 12-, and 18-core biopsies, which accounts for the correlation between proportions. Sensitivity, specificity, positive predictive value, and negative predictive value of biopsy results were calculated using as the standard either the presence of any prostate cancer or of clinically significant cancer, with both obtained from histologic analysis of the whole-mounted prostate. All statistical tests were two-sided, and P values less than .05 were considered to be statistically significant. Statistical analyses were conducted using Stata 9.0 (Stata Corp, College Station, TX). |
Results |
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TopAbstractContext and CaveatsSubjects and MethodsStatistical analysisResultsDiscussionFundingReferencesNotes |
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The 164 prostate glands in our study were from male subjects with a median age of 64 years (interquartile range = 54–73 years). The median gland volume was 40 cm3 (interquartile range = 30–59 cm3) (Table 1).
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Pathologic evaluation identified 47 (29%) prostate cancers and a total of 87 tumor foci (Table 1). The cancers were equally distributed between unifocal (51%) and multifocal (49%). Thirty-three (70%) cancers were well differentiated (Gleason
6), whereas 14 (30%) were Gleason 7 or greater. No statistically significant association was observed between grade and multifocality (P = .6).
Large tumors (0.5 cm3) were less well differentiated than small tumors (<0.5 cm3): 5 of 12 (42%) of the large tumors were Gleason 6 or less, compared with 28 of 35 (80%) of the small tumors (P = .03). In addition, large index tumors (0.5 cm3) were surrounded by more tumor foci than small index tumors (<0.5 cm3). For example, 10 of 12 (83%) of large tumors were surrounded by at least one other tumor foci, compared with only 13 of 35 (37%) of the small tumors (P = .008).
Twenty (43%) cancers were clinically significant. Of these, 13 of 20 (65%) were multifocal, compared with only 10 of 27 (37%) of the clinically insignificant cancers (P = .054).
Prostate cancer prevalence increased with age. The youngest man with cancer detected in the autopsy prostate was aged 42 years. Older men were more likely to have clinically significant cancer (per year of age, odds ratio = 1.07, 95% confidence interval [CI] = 1.03 to 1.10; P<.001) (Fig. 2). For example, only one of 65 (2%) of the men younger than 60 years had a clinically significant cancer, compared with 19 of 98 (19%) of the men aged 60 years and older. The predicted probability of clinically significant prostate cancer increased almost threefold from age 60 to 70 years and then again from age 70 to 80 years. Large tumors (index tumor volume 0.5 cm3) were observed only in men aged 60 years and older. Higher index tumor volume was associated with increased age (P<.001) and higher Gleason score (P = .012). However, we did not find a statistically significant association between tumor multifocality and age (P = .3).
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Needle biopsies detected cancer in 25 of the 47 glands (53%) involved with cancer and in 34 of 87 tumor foci (39%). In one case, two biopsy cores demonstrated cancer; however, the whole-mount analysis did not show any evidence of carcinoma.
We next calculated the sensitivity, specificity, and negative and positive predictive values of the 6-, 12-, and 18-core biopsies (Table 2). Biopsies from the MPZ alone detected 14 prostate cancers (30%, 95% CI = 17% to 45%). Of these, 11 were also detected by either the biopsies taken from the CZ and/or the LPZ. Biopsies from the LPZ alone detected 19 prostate cancers (40%, 95% CI = 26% to 56%), of which eight were detected by biopsies from either the MPZ or the CZ. Biopsies from the CZ alone detected 10 prostate cancers (21%, 95% CI = 11% to 36%), all of which were detected by biopsies from the MPZ and LPZ together (sensitivity 53%, 95% CI = 38% to 68%). The sensitivity of biopsies from the MPZ and LPZ together (i.e., 12-core biopsies) was therefore the same as for all 18-core biopsies and statistically significantly higher than for six-core biopsies from the MPZ alone (P = .003). Because the upper bound of the 95% confidence interval for the sensitivity of the 18-core biopsy was 68%, we were unable to exclude the possibility that an 18-core biopsy improves sensitivity more than that of a 12-core biopsy of MPZ plus LPZ.
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We then compared the sensitivity of biopsies from the MPZ and MPZ plus LPZ relative to tumor volume and clinical significance (Table 3). Biopsies from the MPZ alone detected 11 (55%, 95% CI = 32% to 77%) of the clinically significant and 3 (11%, 95% CI = 2% to 29%) of the clinically insignificant prostate cancers, whereas biopsies from the MPZ and LPZ together detected 16 (80%, 95% CI = 56% to 94%) and 9 (33%, 95% CI = 17% to 54%) of these cancers, respectively (Table 3). Biopsy-detected prostate cancers had higher total tumor volume than those not detected; moreover, more clinically significant cancers were detected than clinically insignificant cancers.
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Discussion |
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TopAbstractContext and CaveatsSubjects and MethodsStatistical analysisResultsDiscussionFundingReferencesNotes |
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The trend among clinicians has been to perform more prostate biopsies to detect more prostate cancers. Sextant biopsies have been all but abandoned, and most studies recommend extended biopsy protocols of 12 cores (18). Some urologists perform saturation biopsies of 32 cores or more in selected patients (19). Our results suggest that the accuracy of prostate cancer detection depends more on the anatomic location from where the biopsies are taken rather than the number of biopsies taken. We detected most cancers in biopsies from the MPZ and LPZ.
Extended biopsy protocols, however, carry a risk of diagnosing clinically insignificant cancers by detecting tumors of lower volume (20). Tumor volume is directly related to the risk of capsular penetration, seminal vesicle invasion, and microscopic metastases to the pelvic lymph nodes (17,21,22). Small and well-differentiated cancers are therefore not thought to be of immediate threat. Epstein et al. (3) and Stamey et al. (4) defined clinically insignificant prostate cancers as organ confined with an index tumor volume less than 0.5 cm3 and a Gleason score of 6 or less.
Several autopsy studies have been used to evaluate the prevalence of prostate cancers among men of various age and racial groups and those who live in distinct geographic areas (7–10,23), but there has not been, to our knowledge, any cancer detection study based on autopsy prostates. Lowering serum PSA concentration cutoff for biopsy has shortened the gap between prostate cancer incidence and prevalence. In the recently completed Prostate Cancer Prevention Trial (PCPT), Thompson et al. (24) noted a fourfold increase of cancer diagnosis in the control population compared with what had been anticipated at the beginning of the trial, and their reported 24% cancer detection rate in patients with normal digital rectal examination and normal PSA level starts to approximate the cancer prevalence rates noted in autopsy studies in similar age groups. The PCPT investigators used sextant biopsies to diagnose cancer; had they used 12-core biopsies, they might have noted a cancer detection rate similar to what was found in this study. Our findings demonstrate that biopsy strategies can be investigated prospectively on autopsy prostates. Unlike clinical studies, which are unable to identify cancers missed by the biopsies, all cancers present in autopsy prostates can be identified and characterized.
In this study, the overall prevalence of prostate cancer was 29%, which is lower than the 36% found in Wayne County, MI, a decade ago (7). Several international studies also showed higher prevalence rates than what we observed, especially among men aged 50–70 years (8,9,23). Demographic differences may explain some of these discrepancies. Also, as suggested by Konety et al. (25), autopsy studies exclude patients who have a history of prostate cancer, and far more men are diagnosed with prostate cancers than previously due to widespread prostate cancer screening. In addition, the thickness of the step sections during prostate processing varies from 2 to 5 mm between autopsy studies (7–10) and may influence the detection of small tumor foci. Thinner step sections may increase the detection of small tumors.
We found statistically significant associations between index tumor volume, total tumor volume, and age, grade, and the number of tumor foci. Gleason score was also associated with age. Small index tumors were well differentiated and associated with fewer secondary tumors. In contrast, prostate cancers with large index tumors were less differentiated and more likely to have secondary tumor foci. Other autopsy studies have reported that prostate cancers with a high Gleason score were more frequently multifocal and that the number of tumor foci increased with age, although these associations were not statistically significant (7,9). Based on these observations, we hypothesize that the first step in the natural history of prostate cancer is the development of a single tumor, followed by the development of additional tumor foci.
This study showed that the sextant biopsies (i.e., in the MPZ alone) missed more than 70% of prostate cancers. Obtaining six additional biopsy cores from the LPZ increased the number of tumor foci detected and the overall sensitivity of cancer detection. However, this increase included both clinically significant and insignificant cancers. Nevertheless, although the number of clinically insignificant cancers detected increased threefold with six additional biopsy cores from the LPZ, the sensitivity remained low (33%). In contrast, the sensitivity for detecting clinically significant cancers increased only 1.45-fold with six additional biopsy cores but reached 80%.
Our study confirms earlier reports that biopsies directed to the CZ have a low likelihood of identifying cancer in the absence of positive biopsies from the PZ of the gland (18,26). The majority of the tumors were located in the PZ, and all the cancers detected by biopsies of the CZ were also detected by either biopsies of the MPZ or the LPZ.
Our study has several limitations. A larger sample size, particularly of men between the ages of 50 and 70 years, who are those subjected to screening in clinical practice, may have resulted in stronger association between biopsy regimens and sensitivity. It should also be noted that the definition of clinical significance does not take into consideration age, comorbidities, and other individual circumstances (11). Furthermore, all the cancers detected in this study would have been clinically insignificant because none of the deceased men was known to have prostate cancer.
In conclusion, adding six LPZ biopsies to the traditional sextant biopsies increased the sensitivity for detecting both clinically significant and insignificant prostate cancer, whereas adding an additional six centrally directed biopsy cores did not appear to increase sensitivity. Most clinically significant cancers were detected, whereas the overall sensitivity for detecting insignificant cancers remained low. This information, put into the context of the clinical characteristics of individual patients, such as overall health and life expectancy, can assist the clinician to design the appropriate biopsy regimen to detect clinically significant cancers that pose biologic risk and avoid the overdiagnosis of clinically insignificant cancers that would be unlikely to have an adverse effect on the patient.
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Funding |
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TopAbstractContext and CaveatsSubjects and MethodsStatistical analysisResultsDiscussionFundingReferencesNotes |
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National Institute On Aging (AG021389 to G. P. H.); National Cancer Institute (CA097751 to G. P. H.); National Institutes of Health (2U42RR006042-13).
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NOTES |
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Dr G. P. Haas had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. H. Lilja holds patents on assays to detect free PSA and prostatic kallikreins in blood.
We acknowledge use of tissues procured by the National Disease Research Interchange with support from National Institutes of Health grant.
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REFERENCES |
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Manuscript received April 10, 2007; revised July 24, 2007; accepted August 13, 2007.
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