Targeted prostate cancer screening in BRCA1 and BRCA2 mutation carriers: results from the initial screening round of the IMPACT study

Elizabeth K Bancroft, Elizabeth C Page, Elena Castro, Hans Lilja, Andrew Vickers, Daniel Sjoberg, Melissa Assel, Christopher S Foster, Gillian Mitchell, Kate Drew, Lovise Mæhle, Karol Axcrona, D Gareth Evans, Barbara Bulman, Diana Eccles, Donna McBride, Christi van Asperen, Hans Vasen, Lambertus A Kiemeney, Janneke Ringelberg, Cezary Cybulski, Dominika Wokolorczyk, Christina Selkirk, Peter J Hulick, Anders Bojesen, Anne-Bine Skytte, Jimmy Lam, Louise Taylor, Rogier Oldenburg, Ruben Cremers, Gerald Verhaegh, Wendy A van Zelst-Stams, Jan C Oosterwijk, Ignacio Blanco, Monica Salinas, Jackie Cook, Derek J Rosario, Saundra Buys, Tom Conner, Margreet G Ausems, Kai-ren Ong, Jonathan Hoffman, Susan Domchek, Jacquelyn Powers, Manuel R Teixeira, Sofia Maia, William D Foulkes, Nassim Taherian, Marielle Ruijs, Apollonia T Helderman-van den Enden, Louise Izatt, Rosemarie Davidson, Muriel A Adank, Lisa Walker, Rita Schmutzler, Kathy Tucker, Judy Kirk, Shirley Hodgson, Marion Harris, Fiona Douglas, Geoffrey J Lindeman, Janez Zgajnar, Marc Tischkowitz, Virginia E Clowes, Rachel Susman, Teresa Ramón y Cajal, Nicholas Patcher, Neus Gadea, Allan Spigelman, Theo van Os, Annelie Liljegren, Lucy Side, Carole Brewer, Angela F Brady, Alan Donaldson, Vigdis Stefansdottir, Eitan Friedman, Rakefet Chen-Shtoyerman, David J Amor, Lucia Copakova, Julian Barwell, Veda N Giri, Vedang Murthy, Nicola Nicolai, Soo-Hwang Teo, Lynn Greenhalgh, Sara Strom, Alex Henderson, John McGrath, David Gallagher, Neil Aaronson, Audrey Ardern-Jones, Chris Bangma, David Dearnaley, Philandra Costello, Jorunn Eyfjord, Jeanette Rothwell, Alison Falconer, Henrik Gronberg, Freddie C Hamdy, Oskar Johannsson, Vincent Khoo, Zsofia Kote-Jarai, Jan Lubinski, Ulrika Axcrona, Jane Melia, Joanne McKinley, Anita V Mitra, Clare Moynihan, Gad Rennert, Mohnish Suri, Penny Wilson, Emma Killick, IMPACT Collaborators, Sue Moss, Rosalind A Eeles, Rosalind Eeles, Elizabeth Bancroft, Elizabeth Page, Elena Castro, Natalie Taylor, Jenny Pope, Sibel Saya, Sue Martin, Diana Keating, Gillian Mitchell, Kate Drew, Joanne McKinley, Lara Petelin, Morgan Murphy, Rebecca Doherty, Sarah Pratt, Gillian Mitchell, Declan Murphy, Laurence Cleeve, Jimmy Lam, Louise Taylor, Cathy Miller, Alan Stapleton, Michael Chong, Graeme Suthers, Katherine Tucker, Lesley Andrews, Jessica Duffy, Katherine Tucker, Richard Millard, Robyn Ward, Rachel Williams, Phillip Stricker, Judy Kirk, Michelle Bowman, Judy Kirk, Manish Patel, Marion Harris, Shona O'Connell, Clare Hunt, Courtney Smyth, Mark Frydenberg, Geoffrey Lindeman, Kylie Shackleton, Geoffrey Lindeman, Geoffrey Lindeman, Rachel Susman, Julie McGaughran, Melanie Boon, Nicholas Pachter, Sharron Townshend, Lyn Schofield, Nicholas Pachter, Allan Spigelman, Margaret Gleeson, Allan Spigelman, Rodney Scott, David Amor, Jo Burke, Briony Patterson, Sonya Bacic, David Amor, Peter Swindle, William Foulkes, Marc Tischkowitz, Nassim Taherian, Armen Aprikian, Anne-Bine Skytte, Anders Bojeson, Dorthe Cruger, Palle Osther, Anne-Marie Gerdes, Rita Schmutzler, Kerstin Rhiem, Kerstin Luedtke-Heckenkamp, Nicole Ochsendorf, Kerstin Fiddike, Oskar Johannsson, Vigdis Stefansdottir, Vedang Murthy, Rajiv Sarin, Kasturi Awatagiri, Sujata Ghonge, Pradnya Kowtal, Gouri Mulgund, David Gallagher, Richard Bambury, Michael Farrell, Fergal Gallagher, Eitan Friedman, Rakefet Chen-Shtoyerman, Sagi Josefsberg Ben-Yehoshua, Rachel Nissani, Zvi Appelman, Evyatar Moriel, Nicola Nicolai, Paolo Radice, Riccardo Valdagni, Tiziana Magnani, Soo Hwang Teo, Hui Meng Tan, Sook-Yee Yoon, Soo Hwang Teo, Meow Keong Thong, Christi van Asperen, Bart Kiemeney, Wendy van Zelst-Stams, Margreet G E M Ausems, Rob B Van der Luijt, Muriel A Adank, Rogier A Oldenburg, Lovise Maehle, Pal Moller, Bjorn Brennhovd, Heidi Medvik, Eldbjørg Hanslien, Theo van Os, Mariëlle W G Ruijs, A Paula T J M Helderman- van den Enden, Jan C Oosterwijk, Cezary Cybulski, Jan Lubinski, Dominika Wokolorczyk, Manuel Teixeira, Sofia Maia, Ana Peixoto, Rui Henrique, Jorge Oliveira, Nuno Gonçalves, Luís Araújo, Manuela Seixas, João Paulo Souto, Pedro Nogueira, Lucia Copakova, Janez Zgajnar, Mateja Krajc, Alenka Vrecar, Ignacio Blanco, Mónica Salinas, Gabriel Capella, Teresa Ramón y Cajal, David Fisas, Judith Balmaña, Neus Gadea, Juan Morote, Annelie Liljegren, Marie Hjälm-Eriksson, Karl-Johan Ekdahl, Stefan Carlsson, Helen Hanson, Susan Shanley, Chee Goh, Emma Killick, Audrey Ardern-Jones, Jennifer Wiggins, Kelly Kohut, Vincent Khoo, Nicholas Van As, Alan Thompson, Chris Ogden, Nigel Borley, Christopher Woodhouse, Pardeep Kumar, D Gareth Evans, Barbara Bulman, Jeanette Rothwell, Diana Eccles, Catherine Mercer, Donna McBride, Philandra Costello, Marc Tischkowitz, Joan Paterson, Virginia Clowes, Amy Taylor, Barbara Newcombe, Lisa Walker, Dorothy Halliday, Barbara Stayner, D Fleming-Brown, Shirley Hodgson, Glen Brice, Tessa Homfray, Carrie Hammond, Carole Brewer, Alison Potter, Caroline Renton, Anne Searle, Kathryn Hill, Selina Goodman, Lynda Garcia, Gemma Devlin, Sarah Everest, Maria Nadolski, Fiona Douglas, Irene Jobson, Edgar Paez, Alan Donaldson, Sue Tomkins, Louise Izatt, Gabriella Pichert, Chris Jacobs, Caroline Langman, Michelle Weston, Angela Brady, Virginia Clowes, Huw Dorkins, Athalie Melville, Monika Kosicka-Slawinska, Carole Cummings, Vicki Kiesel, Marion Bartlett, Kashmir Randhawa, Natalie Ellery, Lucy Side, Alison Male, Kate Simon, Katie Rees, Cecilia Compton, Lizzie Tidey, Jackie Cook, Louise Nevitt, Stuart Ingram, Derek Rosario, James Catto, Joanne Howson, Kai-Ren Ong, Cyril Chapman, Trevor Cole, Tricia Heaton, Jonathan Hoffman, Lucy Burgess, Rosemarie Davidson, Mark Longmuir, Cathy Watt, Alexis Duncan, Julian Barwell, Roger Kockelbergh, Ayisha Sattar, Beckie Kaemba, Zahirah Sidat, Nafisa Patel, Kas Siguake, Alex Henderson, Angela Birt, Una Poultney, Nkem Umez-Eronini, Jaswant Mom, Lynn Greenhalgh, Gillian Roberts, Anthony Woodward, Vivienne Sutton, Philip Cornford, Katy Treherne, Julie Griffiths, Carole Brewer, Lyn Cogley, Christina Selkirk, Peter Hulick, Wendy Rubinstein, Charles Brendler, Brian Helfand, Michael McGuire, Karen Kaul, Daniel Shevrin, Scott Weissman, Anna Newlin, Kristen Vogel, Shelly Weiss, Saundra Buys, David Goldgar, Tom Conner, Vickie Venne, Robert Stephenson, Christopher Dechet, Susan Domchek, Jacquelyn Powers, Sara Strom, Banu Arun, John W Davis, Yuko Yamamura, Veda Giri, Laura Gross, Elizabeth K Bancroft, Elizabeth C Page, Elena Castro, Hans Lilja, Andrew Vickers, Daniel Sjoberg, Melissa Assel, Christopher S Foster, Gillian Mitchell, Kate Drew, Lovise Mæhle, Karol Axcrona, D Gareth Evans, Barbara Bulman, Diana Eccles, Donna McBride, Christi van Asperen, Hans Vasen, Lambertus A Kiemeney, Janneke Ringelberg, Cezary Cybulski, Dominika Wokolorczyk, Christina Selkirk, Peter J Hulick, Anders Bojesen, Anne-Bine Skytte, Jimmy Lam, Louise Taylor, Rogier Oldenburg, Ruben Cremers, Gerald Verhaegh, Wendy A van Zelst-Stams, Jan C Oosterwijk, Ignacio Blanco, Monica Salinas, Jackie Cook, Derek J Rosario, Saundra Buys, Tom Conner, Margreet G Ausems, Kai-ren Ong, Jonathan Hoffman, Susan Domchek, Jacquelyn Powers, Manuel R Teixeira, Sofia Maia, William D Foulkes, Nassim Taherian, Marielle Ruijs, Apollonia T Helderman-van den Enden, Louise Izatt, Rosemarie Davidson, Muriel A Adank, Lisa Walker, Rita Schmutzler, Kathy Tucker, Judy Kirk, Shirley Hodgson, Marion Harris, Fiona Douglas, Geoffrey J Lindeman, Janez Zgajnar, Marc Tischkowitz, Virginia E Clowes, Rachel Susman, Teresa Ramón y Cajal, Nicholas Patcher, Neus Gadea, Allan Spigelman, Theo van Os, Annelie Liljegren, Lucy Side, Carole Brewer, Angela F Brady, Alan Donaldson, Vigdis Stefansdottir, Eitan Friedman, Rakefet Chen-Shtoyerman, David J Amor, Lucia Copakova, Julian Barwell, Veda N Giri, Vedang Murthy, Nicola Nicolai, Soo-Hwang Teo, Lynn Greenhalgh, Sara Strom, Alex Henderson, John McGrath, David Gallagher, Neil Aaronson, Audrey Ardern-Jones, Chris Bangma, David Dearnaley, Philandra Costello, Jorunn Eyfjord, Jeanette Rothwell, Alison Falconer, Henrik Gronberg, Freddie C Hamdy, Oskar Johannsson, Vincent Khoo, Zsofia Kote-Jarai, Jan Lubinski, Ulrika Axcrona, Jane Melia, Joanne McKinley, Anita V Mitra, Clare Moynihan, Gad Rennert, Mohnish Suri, Penny Wilson, Emma Killick, IMPACT Collaborators, Sue Moss, Rosalind A Eeles, Rosalind Eeles, Elizabeth Bancroft, Elizabeth Page, Elena Castro, Natalie Taylor, Jenny Pope, Sibel Saya, Sue Martin, Diana Keating, Gillian Mitchell, Kate Drew, Joanne McKinley, Lara Petelin, Morgan Murphy, Rebecca Doherty, Sarah Pratt, Gillian Mitchell, Declan Murphy, Laurence Cleeve, Jimmy Lam, Louise Taylor, Cathy Miller, Alan Stapleton, Michael Chong, Graeme Suthers, Katherine Tucker, Lesley Andrews, Jessica Duffy, Katherine Tucker, Richard Millard, Robyn Ward, Rachel Williams, Phillip Stricker, Judy Kirk, Michelle Bowman, Judy Kirk, Manish Patel, Marion Harris, Shona O'Connell, Clare Hunt, Courtney Smyth, Mark Frydenberg, Geoffrey Lindeman, Kylie Shackleton, Geoffrey Lindeman, Geoffrey Lindeman, Rachel Susman, Julie McGaughran, Melanie Boon, Nicholas Pachter, Sharron Townshend, Lyn Schofield, Nicholas Pachter, Allan Spigelman, Margaret Gleeson, Allan Spigelman, Rodney Scott, David Amor, Jo Burke, Briony Patterson, Sonya Bacic, David Amor, Peter Swindle, William Foulkes, Marc Tischkowitz, Nassim Taherian, Armen Aprikian, Anne-Bine Skytte, Anders Bojeson, Dorthe Cruger, Palle Osther, Anne-Marie Gerdes, Rita Schmutzler, Kerstin Rhiem, Kerstin Luedtke-Heckenkamp, Nicole Ochsendorf, Kerstin Fiddike, Oskar Johannsson, Vigdis Stefansdottir, Vedang Murthy, Rajiv Sarin, Kasturi Awatagiri, Sujata Ghonge, Pradnya Kowtal, Gouri Mulgund, David Gallagher, Richard Bambury, Michael Farrell, Fergal Gallagher, Eitan Friedman, Rakefet Chen-Shtoyerman, Sagi Josefsberg Ben-Yehoshua, Rachel Nissani, Zvi Appelman, Evyatar Moriel, Nicola Nicolai, Paolo Radice, Riccardo Valdagni, Tiziana Magnani, Soo Hwang Teo, Hui Meng Tan, Sook-Yee Yoon, Soo Hwang Teo, Meow Keong Thong, Christi van Asperen, Bart Kiemeney, Wendy van Zelst-Stams, Margreet G E M Ausems, Rob B Van der Luijt, Muriel A Adank, Rogier A Oldenburg, Lovise Maehle, Pal Moller, Bjorn Brennhovd, Heidi Medvik, Eldbjørg Hanslien, Theo van Os, Mariëlle W G Ruijs, A Paula T J M Helderman- van den Enden, Jan C Oosterwijk, Cezary Cybulski, Jan Lubinski, Dominika Wokolorczyk, Manuel Teixeira, Sofia Maia, Ana Peixoto, Rui Henrique, Jorge Oliveira, Nuno Gonçalves, Luís Araújo, Manuela Seixas, João Paulo Souto, Pedro Nogueira, Lucia Copakova, Janez Zgajnar, Mateja Krajc, Alenka Vrecar, Ignacio Blanco, Mónica Salinas, Gabriel Capella, Teresa Ramón y Cajal, David Fisas, Judith Balmaña, Neus Gadea, Juan Morote, Annelie Liljegren, Marie Hjälm-Eriksson, Karl-Johan Ekdahl, Stefan Carlsson, Helen Hanson, Susan Shanley, Chee Goh, Emma Killick, Audrey Ardern-Jones, Jennifer Wiggins, Kelly Kohut, Vincent Khoo, Nicholas Van As, Alan Thompson, Chris Ogden, Nigel Borley, Christopher Woodhouse, Pardeep Kumar, D Gareth Evans, Barbara Bulman, Jeanette Rothwell, Diana Eccles, Catherine Mercer, Donna McBride, Philandra Costello, Marc Tischkowitz, Joan Paterson, Virginia Clowes, Amy Taylor, Barbara Newcombe, Lisa Walker, Dorothy Halliday, Barbara Stayner, D Fleming-Brown, Shirley Hodgson, Glen Brice, Tessa Homfray, Carrie Hammond, Carole Brewer, Alison Potter, Caroline Renton, Anne Searle, Kathryn Hill, Selina Goodman, Lynda Garcia, Gemma Devlin, Sarah Everest, Maria Nadolski, Fiona Douglas, Irene Jobson, Edgar Paez, Alan Donaldson, Sue Tomkins, Louise Izatt, Gabriella Pichert, Chris Jacobs, Caroline Langman, Michelle Weston, Angela Brady, Virginia Clowes, Huw Dorkins, Athalie Melville, Monika Kosicka-Slawinska, Carole Cummings, Vicki Kiesel, Marion Bartlett, Kashmir Randhawa, Natalie Ellery, Lucy Side, Alison Male, Kate Simon, Katie Rees, Cecilia Compton, Lizzie Tidey, Jackie Cook, Louise Nevitt, Stuart Ingram, Derek Rosario, James Catto, Joanne Howson, Kai-Ren Ong, Cyril Chapman, Trevor Cole, Tricia Heaton, Jonathan Hoffman, Lucy Burgess, Rosemarie Davidson, Mark Longmuir, Cathy Watt, Alexis Duncan, Julian Barwell, Roger Kockelbergh, Ayisha Sattar, Beckie Kaemba, Zahirah Sidat, Nafisa Patel, Kas Siguake, Alex Henderson, Angela Birt, Una Poultney, Nkem Umez-Eronini, Jaswant Mom, Lynn Greenhalgh, Gillian Roberts, Anthony Woodward, Vivienne Sutton, Philip Cornford, Katy Treherne, Julie Griffiths, Carole Brewer, Lyn Cogley, Christina Selkirk, Peter Hulick, Wendy Rubinstein, Charles Brendler, Brian Helfand, Michael McGuire, Karen Kaul, Daniel Shevrin, Scott Weissman, Anna Newlin, Kristen Vogel, Shelly Weiss, Saundra Buys, David Goldgar, Tom Conner, Vickie Venne, Robert Stephenson, Christopher Dechet, Susan Domchek, Jacquelyn Powers, Sara Strom, Banu Arun, John W Davis, Yuko Yamamura, Veda Giri, Laura Gross

Abstract

Background: Men with germline breast cancer 1, early onset (BRCA1) or breast cancer 2, early onset (BRCA2) gene mutations have a higher risk of developing prostate cancer (PCa) than noncarriers. IMPACT (Identification of Men with a genetic predisposition to ProstAte Cancer: Targeted screening in BRCA1/2 mutation carriers and controls) is an international consortium of 62 centres in 20 countries evaluating the use of targeted PCa screening in men with BRCA1/2 mutations.

Objective: To report the first year's screening results for all men at enrollment in the study.

Design, setting and participants: We recruited men aged 40-69 yr with germline BRCA1/2 mutations and a control group of men who have tested negative for a pathogenic BRCA1 or BRCA2 mutation known to be present in their families. All men underwent prostate-specific antigen (PSA) testing at enrollment, and those men with PSA >3 ng/ml were offered prostate biopsy.

Outcome measurements and statistical analysis: PSA levels, PCa incidence, and tumour characteristics were evaluated. The Fisher exact test was used to compare the number of PCa cases among groups and the differences among disease types.

Results and limitations: We recruited 2481 men (791 BRCA1 carriers, 531 BRCA1 controls; 731 BRCA2 carriers, 428 BRCA2 controls). A total of 199 men (8%) presented with PSA >3.0 ng/ml, 162 biopsies were performed, and 59 PCas were diagnosed (18 BRCA1 carriers, 10 BRCA1 controls; 24 BRCA2 carriers, 7 BRCA2 controls); 66% of the tumours were classified as intermediate- or high-risk disease. The positive predictive value (PPV) for biopsy using a PSA threshold of 3.0 ng/ml in BRCA2 mutation carriers was 48%-double the PPV reported in population screening studies. A significant difference in detecting intermediate- or high-risk disease was observed in BRCA2 carriers. Ninety-five percent of the men were white, thus the results cannot be generalised to all ethnic groups.

Conclusions: The IMPACT screening network will be useful for targeted PCa screening studies in men with germline genetic risk variants as they are discovered. These preliminary results support the use of targeted PSA screening based on BRCA genotype and show that this screening yields a high proportion of aggressive disease.

Patient summary: In this report, we demonstrate that germline genetic markers can be used to identify men at higher risk of prostate cancer. Targeting screening at these men resulted in the identification of tumours that were more likely to require treatment.

Keywords: BRCA1; BRCA2; Prostate cancer; Prostate-specific antigen; Targeted screening.

Copyright © 2014 European Association of Urology. All rights reserved.

Figures

Fig. 1
Fig. 1
Study design. ASAP = atypical small acinar proliferation; PIN = prostate intraepithelial neoplasia; PSA = prostate-specific antigen; QoL = quality-of-life.
Fig. 2
Fig. 2
Consort diagram for the first round of screening. BRCA1 = breast cancer 1, early onset; BRCA2 = breast cancer 2, early onset; PSA = prostate-specific antigen; PPV = positive predictive value. * Controls were men who had a negative predictive genetic test for the BRCA mutation in their family.

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