Comparative analysis of biopsy upgrading in four prostate cancer active surveillance cohorts

Lurdes Y.T. Inoue; Daniel W. Lin; Lisa F. Newcomb; Amy S. Leonardson; Donna Ankerst; Roman Gulati; H. Ballentine Carter; Bruce J. Trock; Peter R. Carroll; Matthew R. Cooperberg; Janet E. Cowan; Laurence H. Klotz; Alexandre Mamedov; David F. Penson; Ruth Etzioni

doi:10.7326/M17-0548

Comparative analysis of biopsy upgrading in four prostate cancer active surveillance cohorts

Lurdes Y.T. Inoue, Daniel W. Lin, Lisa F. Newcomb, Amy S. Leonardson, Donna Ankerst, Roman Gulati, H. Ballentine Carter, Bruce J. Trock, Peter R. Carroll, Matthew R. Cooperberg, Janet E. Cowan, Laurence H. Klotz, Alexandre Mamedov, David F. Penson, Ruth Etzioni

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Abstract

Background: Active surveillance (AS) is increasingly accepted for managing low-risk prostate cancer, yet there is no consensus about implementation. This lack of consensus is due in part to uncertainty about risks for disease progression, which have not been systematically compared or integrated across AS studies with variable surveillance protocols and dropout to active treatment. Objective: To compare risks for upgrading from a Gleason score (GS) of 6 or less to 7 or more across AS studies after accounting for differences in surveillance intervals and competing treatments and to evaluate tradeoffs of more versus less frequent biopsies. Design: Joint statistical model of longitudinal prostate-specific antigen (PSA) levels and risks for biopsy upgrading. Setting: Johns Hopkins University (JHU); Canary Prostate Active Surveillance Study (PASS); University of California, San Francisco (UCSF); and University of Toronto (UT) AS studies. Patients: 2576 men aged 40 to 80 years with a GS between 2 and 6 and clinical stage T1 or T2 prostate cancer enrolled between 1995 and 2014.

Measurements: PSA levels and biopsy GSs. Results: After variable surveillance intervals and competing treatments were accounted for, estimated risks for biopsy upgrading were similar in the PASS and UT studies but higher in UCSF and lower in JHU studies. All cohorts had a delay of 3 to 5 months in detecting upgrading with biennial biopsies starting after a first confirmatory biopsy versus annual biopsies. Limitation: The model does not account for possible misclassification of biopsy GS. Conclusion: Men in different AS studies have different risks for biopsy upgrading after variable surveillance protocols and competing treatments are accounted for. Despite these differences, the consequences of more versus less frequent biopsies seem to be similar across cohorts. Biennial biopsies seem to be an acceptable alternative to annual biopsies. Primary Funding Source: National Cancer Institute.

Original language	English (US)
Pages (from-to)	1-9
Number of pages	9
Journal	Annals of internal medicine
Volume	168
Issue number	1
DOIs	https://doi.org/10.7326/M17-0548
State	Published - Jan 2 2018
Externally published	Yes

ASJC Scopus subject areas

Internal Medicine

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Inoue, L. Y. T., Lin, D. W., Newcomb, L. F., Leonardson, A. S., Ankerst, D., Gulati, R., Carter, H. B., Trock, B. J., Carroll, P. R., Cooperberg, M. R., Cowan, J. E., Klotz, L. H., Mamedov, A., Penson, D. F., & Etzioni, R. (2018). Comparative analysis of biopsy upgrading in four prostate cancer active surveillance cohorts. Annals of internal medicine, 168(1), 1-9. https://doi.org/10.7326/M17-0548

Inoue, LYT, Lin, DW, Newcomb, LF, Leonardson, AS, Ankerst, D, Gulati, R, Carter, HB, Trock, BJ, Carroll, PR, Cooperberg, MR, Cowan, JE, Klotz, LH, Mamedov, A, Penson, DF & Etzioni, R 2018, 'Comparative analysis of biopsy upgrading in four prostate cancer active surveillance cohorts', Annals of internal medicine, vol. 168, no. 1, pp. 1-9. https://doi.org/10.7326/M17-0548

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title = "Comparative analysis of biopsy upgrading in four prostate cancer active surveillance cohorts",

abstract = "Background: Active surveillance (AS) is increasingly accepted for managing low-risk prostate cancer, yet there is no consensus about implementation. This lack of consensus is due in part to uncertainty about risks for disease progression, which have not been systematically compared or integrated across AS studies with variable surveillance protocols and dropout to active treatment. Objective: To compare risks for upgrading from a Gleason score (GS) of 6 or less to 7 or more across AS studies after accounting for differences in surveillance intervals and competing treatments and to evaluate tradeoffs of more versus less frequent biopsies. Design: Joint statistical model of longitudinal prostate-specific antigen (PSA) levels and risks for biopsy upgrading. Setting: Johns Hopkins University (JHU); Canary Prostate Active Surveillance Study (PASS); University of California, San Francisco (UCSF); and University of Toronto (UT) AS studies. Patients: 2576 men aged 40 to 80 years with a GS between 2 and 6 and clinical stage T1 or T2 prostate cancer enrolled between 1995 and 2014.Measurements: PSA levels and biopsy GSs. Results: After variable surveillance intervals and competing treatments were accounted for, estimated risks for biopsy upgrading were similar in the PASS and UT studies but higher in UCSF and lower in JHU studies. All cohorts had a delay of 3 to 5 months in detecting upgrading with biennial biopsies starting after a first confirmatory biopsy versus annual biopsies. Limitation: The model does not account for possible misclassification of biopsy GS. Conclusion: Men in different AS studies have different risks for biopsy upgrading after variable surveillance protocols and competing treatments are accounted for. Despite these differences, the consequences of more versus less frequent biopsies seem to be similar across cohorts. Biennial biopsies seem to be an acceptable alternative to annual biopsies. Primary Funding Source: National Cancer Institute.",

author = "Inoue, {Lurdes Y.T.} and Lin, {Daniel W.} and Newcomb, {Lisa F.} and Leonardson, {Amy S.} and Donna Ankerst and Roman Gulati and Carter, {H. Ballentine} and Trock, {Bruce J.} and Carroll, {Peter R.} and Cooperberg, {Matthew R.} and Cowan, {Janet E.} and Klotz, {Laurence H.} and Alexandre Mamedov and Penson, {David F.} and Ruth Etzioni",

note = "Funding Information: Disclosures: Dr. Trock reports grants from MDxHealth, personal fees from GenomeDx Biosciences, and grants and personal fees from Myriad Genetics outside the submitted work. Dr. Cooperberg reports personal fees from Dendreon, Astel-las, GenomeDx, Myriad Genetics, and MDxHealth outside the submitted work. Ms. Cowan reports that she is a paid statistical peer reviewer for Journal of Urology and Urology. Dr. Pen-son reports grants from the National Cancer Institute at the National Institutes of Health during the conduct of the study. Authors not named here have disclosed no conflicts of interest. Disclosures can also be viewed at www.acponline.org /authors/icmje/ConflictOfInterestForms.do?msNum=M17 -0548. Funding Information: Financial Support: By National Cancer Institute awards R01 CA183570 for the Prostate Modeling to Identify Surveillance Strategies (PROMISS) consortium (all authors), R01 CA160239 for statistical methods to study cancer recurrence using longitudinal multistate models (Dr. Inoue), P50 CA097186 as part of the Pacific Northwest Prostate Cancer Specialized Program of Research Excellence (Ms. Leonardson), and U01 CA199338 as part of the Cancer Intervention and Surveillance Modeling Network (CISNET) (Mr. Gulati and Dr. Etzioni); the Canary Foundation (Drs. Lin and Newcomb); Genomic Health and U.S. Department of Defense Translational Impact Award for Prostate Cancer award W81XWH-13-2-0074 (Drs. Carroll and Cooperberg and Ms. Cowan); and Prostate Cancer Canada (Dr. Klotz).",

year = "2018",

month = jan,

day = "2",

doi = "10.7326/M17-0548",

language = "English (US)",

volume = "168",

pages = "1--9",

journal = "Annals of internal medicine",

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publisher = "American College of Physicians",

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TY - JOUR

T1 - Comparative analysis of biopsy upgrading in four prostate cancer active surveillance cohorts

AU - Inoue, Lurdes Y.T.

AU - Lin, Daniel W.

AU - Newcomb, Lisa F.

AU - Leonardson, Amy S.

AU - Ankerst, Donna

AU - Gulati, Roman

AU - Carter, H. Ballentine

AU - Trock, Bruce J.

AU - Carroll, Peter R.

AU - Cooperberg, Matthew R.

AU - Cowan, Janet E.

AU - Klotz, Laurence H.

AU - Mamedov, Alexandre

AU - Penson, David F.

AU - Etzioni, Ruth

N1 - Funding Information: Disclosures: Dr. Trock reports grants from MDxHealth, personal fees from GenomeDx Biosciences, and grants and personal fees from Myriad Genetics outside the submitted work. Dr. Cooperberg reports personal fees from Dendreon, Astel-las, GenomeDx, Myriad Genetics, and MDxHealth outside the submitted work. Ms. Cowan reports that she is a paid statistical peer reviewer for Journal of Urology and Urology. Dr. Pen-son reports grants from the National Cancer Institute at the National Institutes of Health during the conduct of the study. Authors not named here have disclosed no conflicts of interest. Disclosures can also be viewed at www.acponline.org /authors/icmje/ConflictOfInterestForms.do?msNum=M17 -0548. Funding Information: Financial Support: By National Cancer Institute awards R01 CA183570 for the Prostate Modeling to Identify Surveillance Strategies (PROMISS) consortium (all authors), R01 CA160239 for statistical methods to study cancer recurrence using longitudinal multistate models (Dr. Inoue), P50 CA097186 as part of the Pacific Northwest Prostate Cancer Specialized Program of Research Excellence (Ms. Leonardson), and U01 CA199338 as part of the Cancer Intervention and Surveillance Modeling Network (CISNET) (Mr. Gulati and Dr. Etzioni); the Canary Foundation (Drs. Lin and Newcomb); Genomic Health and U.S. Department of Defense Translational Impact Award for Prostate Cancer award W81XWH-13-2-0074 (Drs. Carroll and Cooperberg and Ms. Cowan); and Prostate Cancer Canada (Dr. Klotz).

PY - 2018/1/2

Y1 - 2018/1/2

N2 - Background: Active surveillance (AS) is increasingly accepted for managing low-risk prostate cancer, yet there is no consensus about implementation. This lack of consensus is due in part to uncertainty about risks for disease progression, which have not been systematically compared or integrated across AS studies with variable surveillance protocols and dropout to active treatment. Objective: To compare risks for upgrading from a Gleason score (GS) of 6 or less to 7 or more across AS studies after accounting for differences in surveillance intervals and competing treatments and to evaluate tradeoffs of more versus less frequent biopsies. Design: Joint statistical model of longitudinal prostate-specific antigen (PSA) levels and risks for biopsy upgrading. Setting: Johns Hopkins University (JHU); Canary Prostate Active Surveillance Study (PASS); University of California, San Francisco (UCSF); and University of Toronto (UT) AS studies. Patients: 2576 men aged 40 to 80 years with a GS between 2 and 6 and clinical stage T1 or T2 prostate cancer enrolled between 1995 and 2014.Measurements: PSA levels and biopsy GSs. Results: After variable surveillance intervals and competing treatments were accounted for, estimated risks for biopsy upgrading were similar in the PASS and UT studies but higher in UCSF and lower in JHU studies. All cohorts had a delay of 3 to 5 months in detecting upgrading with biennial biopsies starting after a first confirmatory biopsy versus annual biopsies. Limitation: The model does not account for possible misclassification of biopsy GS. Conclusion: Men in different AS studies have different risks for biopsy upgrading after variable surveillance protocols and competing treatments are accounted for. Despite these differences, the consequences of more versus less frequent biopsies seem to be similar across cohorts. Biennial biopsies seem to be an acceptable alternative to annual biopsies. Primary Funding Source: National Cancer Institute.

AB - Background: Active surveillance (AS) is increasingly accepted for managing low-risk prostate cancer, yet there is no consensus about implementation. This lack of consensus is due in part to uncertainty about risks for disease progression, which have not been systematically compared or integrated across AS studies with variable surveillance protocols and dropout to active treatment. Objective: To compare risks for upgrading from a Gleason score (GS) of 6 or less to 7 or more across AS studies after accounting for differences in surveillance intervals and competing treatments and to evaluate tradeoffs of more versus less frequent biopsies. Design: Joint statistical model of longitudinal prostate-specific antigen (PSA) levels and risks for biopsy upgrading. Setting: Johns Hopkins University (JHU); Canary Prostate Active Surveillance Study (PASS); University of California, San Francisco (UCSF); and University of Toronto (UT) AS studies. Patients: 2576 men aged 40 to 80 years with a GS between 2 and 6 and clinical stage T1 or T2 prostate cancer enrolled between 1995 and 2014.Measurements: PSA levels and biopsy GSs. Results: After variable surveillance intervals and competing treatments were accounted for, estimated risks for biopsy upgrading were similar in the PASS and UT studies but higher in UCSF and lower in JHU studies. All cohorts had a delay of 3 to 5 months in detecting upgrading with biennial biopsies starting after a first confirmatory biopsy versus annual biopsies. Limitation: The model does not account for possible misclassification of biopsy GS. Conclusion: Men in different AS studies have different risks for biopsy upgrading after variable surveillance protocols and competing treatments are accounted for. Despite these differences, the consequences of more versus less frequent biopsies seem to be similar across cohorts. Biennial biopsies seem to be an acceptable alternative to annual biopsies. Primary Funding Source: National Cancer Institute.

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Comparative analysis of biopsy upgrading in four prostate cancer active surveillance cohorts

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