Storage Time and DNA Quality Determine BRCA1/2 Sequencing Success in Prostate Cancer: A Multicentre Analysis with Therapeutic Implications
Background: Approximately 25.0% of metastatic prostate cancer patients harbour DNA damage repair mutations, including BRCA1 and BRCA2, which are actionable targets for poly(ADP-ribose) polymerase (PARP) inhibitors. Accurate detection of BRCA1/2 mutations is critical for guiding targeted therapies, b...
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| Veröffentlicht in: | Cancers Jg. 17; H. 10; S. 1705 |
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20.05.2025
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| Abstract | Background: Approximately 25.0% of metastatic prostate cancer patients harbour DNA damage repair mutations, including BRCA1 and BRCA2, which are actionable targets for poly(ADP-ribose) polymerase (PARP) inhibitors. Accurate detection of BRCA1/2 mutations is critical for guiding targeted therapies, but crucial pre-analytical factors, such as tissue storage duration and DNA fragmentation, drastically affect the reliability of next-generation sequencing (NGS) using real-world diagnostic specimens. Methods: This multicentre study analysed 954 formalin-fixed paraffin-embedded tissue samples from 11 centres, including 559 biopsies and 395 surgical specimens. This study examined the impact of storage duration (<1 year, 1–2 years, and >2 years) and DNA parameters (concentration and fragmentation index) on NGS success rates. Logistic regression and Cox regression analyses were used to assess correlations between these factors and sequencing outcomes. Results: NGS success rates decreased significantly with longer storage, from 87.8% (<1 year) to 69.1% (>2 years). Samples with higher DNA concentrations and fragmentation indexes had higher success rates (p < 0.001). Surgical specimens had superior success rates (83.3%) compared with biopsies (72.8%) due to better DNA quality. The DNA degradation rate was more pronounced in older samples, underscoring the negative impact of extended storage. Conclusions: Timely testing of BRCA1/2 mutations is critical for optimizing the identification of prostate cancer patients eligible for PARP inhibitors. Surgical specimens provide more reliable results than biopsies and minimizing the storage duration significantly enhances testing outcomes. Standardizing pre-analytical and laboratory procedures across centres is essential to ensure personalized treatments and improve patient outcomes. |
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| AbstractList | Timely detection of BRCA1/2 mutations is essential for identifying metastatic prostate cancer patients who may benefit from PARP inhibitor therapy. However, pre-analytical factors, such as storage time and sample quality, significantly affect sequencing success. In this large multicentre study, we found that prolonged storage time, lower DNA concentration, and biopsy specimens were associated with reduced success rates for BRCA testing. Our findings support the need for early molecular testing and standardized tissue handling protocols to improve patient eligibility for targeted therapies. Approximately 25.0% of metastatic prostate cancer patients harbour DNA damage repair mutations, including BRCA1 and BRCA2, which are actionable targets for poly(ADP-ribose) polymerase (PARP) inhibitors. Accurate detection of BRCA1/2 mutations is critical for guiding targeted therapies, but crucial pre-analytical factors, such as tissue storage duration and DNA fragmentation, drastically affect the reliability of next-generation sequencing (NGS) using real-world diagnostic specimens.BACKGROUNDApproximately 25.0% of metastatic prostate cancer patients harbour DNA damage repair mutations, including BRCA1 and BRCA2, which are actionable targets for poly(ADP-ribose) polymerase (PARP) inhibitors. Accurate detection of BRCA1/2 mutations is critical for guiding targeted therapies, but crucial pre-analytical factors, such as tissue storage duration and DNA fragmentation, drastically affect the reliability of next-generation sequencing (NGS) using real-world diagnostic specimens.This multicentre study analysed 954 formalin-fixed paraffin-embedded tissue samples from 11 centres, including 559 biopsies and 395 surgical specimens. This study examined the impact of storage duration (<1 year, 1-2 years, and >2 years) and DNA parameters (concentration and fragmentation index) on NGS success rates. Logistic regression and Cox regression analyses were used to assess correlations between these factors and sequencing outcomes.METHODSThis multicentre study analysed 954 formalin-fixed paraffin-embedded tissue samples from 11 centres, including 559 biopsies and 395 surgical specimens. This study examined the impact of storage duration (<1 year, 1-2 years, and >2 years) and DNA parameters (concentration and fragmentation index) on NGS success rates. Logistic regression and Cox regression analyses were used to assess correlations between these factors and sequencing outcomes.NGS success rates decreased significantly with longer storage, from 87.8% (<1 year) to 69.1% (>2 years). Samples with higher DNA concentrations and fragmentation indexes had higher success rates (p < 0.001). Surgical specimens had superior success rates (83.3%) compared with biopsies (72.8%) due to better DNA quality. The DNA degradation rate was more pronounced in older samples, underscoring the negative impact of extended storage.RESULTSNGS success rates decreased significantly with longer storage, from 87.8% (<1 year) to 69.1% (>2 years). Samples with higher DNA concentrations and fragmentation indexes had higher success rates (p < 0.001). Surgical specimens had superior success rates (83.3%) compared with biopsies (72.8%) due to better DNA quality. The DNA degradation rate was more pronounced in older samples, underscoring the negative impact of extended storage.Timely testing of BRCA1/2 mutations is critical for optimizing the identification of prostate cancer patients eligible for PARP inhibitors. Surgical specimens provide more reliable results than biopsies and minimizing the storage duration significantly enhances testing outcomes. Standardizing pre-analytical and laboratory procedures across centres is essential to ensure personalized treatments and improve patient outcomes.CONCLUSIONSTimely testing of BRCA1/2 mutations is critical for optimizing the identification of prostate cancer patients eligible for PARP inhibitors. Surgical specimens provide more reliable results than biopsies and minimizing the storage duration significantly enhances testing outcomes. Standardizing pre-analytical and laboratory procedures across centres is essential to ensure personalized treatments and improve patient outcomes. Background: Approximately 25.0% of metastatic prostate cancer patients harbour DNA damage repair mutations, including BRCA1 and BRCA2, which are actionable targets for poly(ADP-ribose) polymerase (PARP) inhibitors. Accurate detection of BRCA1/2 mutations is critical for guiding targeted therapies, but crucial pre-analytical factors, such as tissue storage duration and DNA fragmentation, drastically affect the reliability of next-generation sequencing (NGS) using real-world diagnostic specimens. Methods: This multicentre study analysed 954 formalin-fixed paraffin-embedded tissue samples from 11 centres, including 559 biopsies and 395 surgical specimens. This study examined the impact of storage duration (<1 year, 1–2 years, and >2 years) and DNA parameters (concentration and fragmentation index) on NGS success rates. Logistic regression and Cox regression analyses were used to assess correlations between these factors and sequencing outcomes. Results: NGS success rates decreased significantly with longer storage, from 87.8% (<1 year) to 69.1% (>2 years). Samples with higher DNA concentrations and fragmentation indexes had higher success rates (p < 0.001). Surgical specimens had superior success rates (83.3%) compared with biopsies (72.8%) due to better DNA quality. The DNA degradation rate was more pronounced in older samples, underscoring the negative impact of extended storage. Conclusions: Timely testing of BRCA1/2 mutations is critical for optimizing the identification of prostate cancer patients eligible for PARP inhibitors. Surgical specimens provide more reliable results than biopsies and minimizing the storage duration significantly enhances testing outcomes. Standardizing pre-analytical and laboratory procedures across centres is essential to ensure personalized treatments and improve patient outcomes. Timely detection of BRCA1/2 mutations is essential for identifying metastatic prostate cancer patients who may benefit from PARP inhibitor therapy. However, pre-analytical factors, such as storage time and sample quality, significantly affect sequencing success. In this large multicentre study, we found that prolonged storage time, lower DNA concentration, and biopsy specimens were associated with reduced success rates for BRCA testing. Our findings support the need for early molecular testing and standardized tissue handling protocols to improve patient eligibility for targeted therapies. Background: Approximately 25.0% of metastatic prostate cancer patients harbour DNA damage repair mutations, including BRCA1 and BRCA2, which are actionable targets for poly(ADP-ribose) polymerase (PARP) inhibitors. Accurate detection of BRCA1/2 mutations is critical for guiding targeted therapies, but crucial pre-analytical factors, such as tissue storage duration and DNA fragmentation, drastically affect the reliability of next-generation sequencing (NGS) using real-world diagnostic specimens. Methods: This multicentre study analysed 954 formalin-fixed paraffin-embedded tissue samples from 11 centres, including 559 biopsies and 395 surgical specimens. This study examined the impact of storage duration (<1 year, 1–2 years, and >2 years) and DNA parameters (concentration and fragmentation index) on NGS success rates. Logistic regression and Cox regression analyses were used to assess correlations between these factors and sequencing outcomes. Results: NGS success rates decreased significantly with longer storage, from 87.8% (<1 year) to 69.1% (>2 years). Samples with higher DNA concentrations and fragmentation indexes had higher success rates (p < 0.001). Surgical specimens had superior success rates (83.3%) compared with biopsies (72.8%) due to better DNA quality. The DNA degradation rate was more pronounced in older samples, underscoring the negative impact of extended storage. Conclusions: Timely testing of BRCA1/2 mutations is critical for optimizing the identification of prostate cancer patients eligible for PARP inhibitors. Surgical specimens provide more reliable results than biopsies and minimizing the storage duration significantly enhances testing outcomes. Standardizing pre-analytical and laboratory procedures across centres is essential to ensure personalized treatments and improve patient outcomes. Approximately 25.0% of metastatic prostate cancer patients harbour DNA damage repair mutations, including and , which are actionable targets for poly(ADP-ribose) polymerase (PARP) inhibitors. Accurate detection of /2 mutations is critical for guiding targeted therapies, but crucial pre-analytical factors, such as tissue storage duration and DNA fragmentation, drastically affect the reliability of next-generation sequencing (NGS) using real-world diagnostic specimens. This multicentre study analysed 954 formalin-fixed paraffin-embedded tissue samples from 11 centres, including 559 biopsies and 395 surgical specimens. This study examined the impact of storage duration (<1 year, 1-2 years, and >2 years) and DNA parameters (concentration and fragmentation index) on NGS success rates. Logistic regression and Cox regression analyses were used to assess correlations between these factors and sequencing outcomes. NGS success rates decreased significantly with longer storage, from 87.8% (<1 year) to 69.1% (>2 years). Samples with higher DNA concentrations and fragmentation indexes had higher success rates ( < 0.001). Surgical specimens had superior success rates (83.3%) compared with biopsies (72.8%) due to better DNA quality. The DNA degradation rate was more pronounced in older samples, underscoring the negative impact of extended storage. Timely testing of /2 mutations is critical for optimizing the identification of prostate cancer patients eligible for PARP inhibitors. Surgical specimens provide more reliable results than biopsies and minimizing the storage duration significantly enhances testing outcomes. Standardizing pre-analytical and laboratory procedures across centres is essential to ensure personalized treatments and improve patient outcomes. |
| Audience | Academic |
| Author | Giunchi, Francesca Conversano, Federica Fassan, Matteo de Biase, Dario Tommasi, Stefania Seminati, Davide Malapelle, Umberto Caputo, Alessandro Nardi, Eleonora Pepe, Francesco Vecchione, Andrea Carosi, Mariantonia Perrone, Giuseppe Scarpino, Stefania Rappa, Alessandra Zeppa, Pio Taffon, Chiara Righi, Daniela Guerini-Rocco, Elena Nibid, Lorenzo Gaeta, Sara Massari, Francesco Melucci, Elisa Casini, Beatrice Toffolatti, Luisa Troncone, Giancarlo Prata, Francesco Raspollini, Maria Rosaria Pagni, Fabio Coppola, Claudio Antonio Castiglione, Francesca Vescovo, Mariavittoria |
| AuthorAffiliation | 3 Research Unit of Anatomical Pathology, Department of Medicine and Surgery, Università Campus Bio-Medico di Roma, Via Alvaro del Portillo, 21, 00128 Rome, Italy 9 Department of Public Health, University Federico II of Naples, 80131 Naples, Italy; pepefrancesco88@yahoo.it (F.P.); giancarlo.troncone@unina.it (G.T.); umbertomalapelle@gmail.com (U.M.) 4 Solid Tumor Molecular Pathology Laboratory, IRCCS Azienda Ospedaliero-Universitaria di Bologna, 40138 Bologna, Italy; dario.debiase@unibo.it 19 Department of Medicine and Surgery, University Milan Bicocca and Fondazione IRCCS San Gerardo dei Tintori Monza, 20126 Milan, Italy; fabio.pagni@unimib.it (F.P.) 20 Unit of Pathology, Department of Clinical and Molecular Medicine, Sant’Andrea Hospital, Sapienza University, 00189 Rome, Italy; andrea.vecchione@uniroma1.it (A.V.); stefania.scarpino@uniroma1.it (S.S.) 1 Anatomical Pathology Operative Research Unit, Fondazione Policlinico Universitario Campus Bio-Medico, Via Alvaro del Portillo, 200, 00128 R |
| AuthorAffiliation_xml | – name: 7 Department of Medical and Surgical Sciences (DIMEC), University of Bologna, 40138 Bologna, Italy – name: 19 Department of Medicine and Surgery, University Milan Bicocca and Fondazione IRCCS San Gerardo dei Tintori Monza, 20126 Milan, Italy; fabio.pagni@unimib.it (F.P.) – name: 8 Pathology Unit, IRCCS Azienda Ospedaliero-Universitaria di Bologna, 40138 Bologna, Italy; francesca.giunchi@aosp.bo.it – name: 21 Department of Urology, Fondazione Policlinico Universitario Campus Bio-Medico, 00128 Rome, Italy; f.prata@policlinicocampus.it – name: 5 Department of Pharmacy and Biotechnology, University of Bologna, 40126 Bologna, Italy – name: 9 Department of Public Health, University Federico II of Naples, 80131 Naples, Italy; pepefrancesco88@yahoo.it (F.P.); giancarlo.troncone@unina.it (G.T.); umbertomalapelle@gmail.com (U.M.) – name: 14 Department of Oncology and Hemato-Oncology, University of Milan, 20122 Milan, Italy; elena.guerinirocco@ieo.it – name: 3 Research Unit of Anatomical Pathology, Department of Medicine and Surgery, Università Campus Bio-Medico di Roma, Via Alvaro del Portillo, 21, 00128 Rome, Italy – name: 1 Anatomical Pathology Operative Research Unit, Fondazione Policlinico Universitario Campus Bio-Medico, Via Alvaro del Portillo, 200, 00128 Rome, Italy; lorenzo.nibid@unicampus.it (L.N.); d.righi@policlinicocampus.it (D.R.); c.taffon@policlinicocampus.it (C.T.); g.perrone@policlinicocampus.it (G.P.) – name: 2 Histopathology and Molecular Diagnostics, University Hospital Careggi, Via Pieraccini, 6, 50129 Florence, Italy; mariarosaria.raspollini@aouc.unifi.it (M.R.R.); francesca.castiglione@gmail.com (F.C.); eleonora.nardi@unifi.it (E.N.) – name: 6 Medical Oncology, IRCCS Azienda Ospedaliero-Universitaria di Bologna, 40138 Bologna, Italy; francesco.massari8@unibo.it – name: 10 Molecular Diagnostic Laboratory, Pathology Department, Advanced Diagnostics Research and Technological Innovation Department, Regina, Elena National Cancer Institute, Via Elio Chianesi, 53, 00144 Rome, Italy; mariantonia.carosi@ifo.it (M.C.); beatrice.casini@ifo.it (B.C.); elisa.melucci@ifo.it (E.M.) – name: 16 Pharmacogenetics and Molecular Diagnostics Unit, IRCCS Istituto Tumori Giovanni Paolo II Bari, 70124 Bari, Italy; stefania.tommasi@gmail.com (S.T.); c.a.coppola@oncologico.bari.it (C.A.C.) – name: 12 Veneto Institute of Oncology (IOV-IRCCS), 35128 Padua, Italy – name: 13 Surgical Pathology Unit, Ca’ Foncello General Hospital, ULSS2 Marca Trevigiana, 31100 Treviso, Italy; luisa.toffolatti@aulss2.veneto.it – name: 20 Unit of Pathology, Department of Clinical and Molecular Medicine, Sant’Andrea Hospital, Sapienza University, 00189 Rome, Italy; andrea.vecchione@uniroma1.it (A.V.); stefania.scarpino@uniroma1.it (S.S.) – name: 17 Department of Medicine, Surgery, and Dentistry “Scuola Medica Salernitana”, University of Salerno, 84084 Baronissi, Italy; p.zeppa@unisa.it (P.Z.); alessandro.caputo94@gmail.com (A.C.) – name: 18 Department of Pathology, University Hospital of Salerno, 84081 Salerno, Italy; sara.gaeta@sangiovannieruggi.it – name: 4 Solid Tumor Molecular Pathology Laboratory, IRCCS Azienda Ospedaliero-Universitaria di Bologna, 40138 Bologna, Italy; dario.debiase@unibo.it – name: 15 Division of Pathology, European Institute of Oncology, IRCCS, 20141 Milan, Italy; federica.conversano@ieo.it (F.C.); alessandra.rappa@ieo.it (A.R.) – name: 11 Department of Medicine (DIMED), University of Padua, 35122 Padua, Italy; matteo.fassan@gmail.com |
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| Keywords | BRCA1/2 NGS analysis metastatic castration resistant prostate cancer storage time target therapy |
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| PublicationDate_xml | – month: 05 year: 2025 text: 2025-05-20 day: 20 |
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| PublicationTitle | Cancers |
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| PublicationYear | 2025 |
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| References | Castro (ref_27) 2019; 37 Fan (ref_29) 2024; 41 Scott (ref_30) 2021; 12 Zannini (ref_9) 2023; 243 Hiemenz (ref_22) 2022; 27 Gonzalez (ref_24) 2021; 7 Giri (ref_7) 2018; 78 ref_12 Wallace (ref_25) 2016; 24 Paul (ref_6) 2014; 19 Tuffaha (ref_14) 2024; 27 Rehm (ref_21) 2013; 15 Pommier (ref_15) 2016; 8 Giannini (ref_19) 2011; 135 Mateo (ref_10) 2020; 382 Tappero (ref_3) 2024; 22 Mafficini (ref_16) 2016; 7 ref_23 Ferriero (ref_13) 2024; 27 Capoluongo (ref_26) 2017; 44 ref_1 Tommasi (ref_20) 2024; 116 Leith (ref_28) 2022; 18 ref_2 ref_8 Akhoundova (ref_4) 2024; 31 ref_5 Mateo (ref_11) 2015; 373 Hussain (ref_18) 2022; 28 Zannini (ref_17) 2025; 266 |
| References_xml | – volume: 24 start-page: S10 year: 2016 ident: ref_25 article-title: New Challenges for BRCA Testing: A View from the Diagnostic Laboratory publication-title: Eur. J. Hum. Genet. doi: 10.1038/ejhg.2016.94 – volume: 22 start-page: 47 year: 2024 ident: ref_3 article-title: Overall Survival of Metastatic Prostate Cancer Patients According to Location of Visceral Metastatic Sites publication-title: Clin. Genitourin. Cancer doi: 10.1016/j.clgc.2023.08.004 – ident: ref_5 doi: 10.3390/ijms222312628 – ident: ref_8 doi: 10.3390/cancers15092435 – volume: 116 start-page: 303 year: 2024 ident: ref_20 article-title: BRCA Testing in Metastatic Castration-Resistant Prostate Cancer: Successes and Troubles in a Real World Setting. An Italian Multicentric Study publication-title: Pathol.—J. Ital. Soc. Anat. Pathol. Diagn. 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Anat. Pathol. doi: 10.1097/PAP.0000000000000422 – volume: 41 start-page: 2196 year: 2024 ident: ref_29 article-title: Homologous Recombination Repair Gene Mutations in Prostate Cancer: Prevalence and Clinical Value publication-title: Adv. Ther. doi: 10.1007/s12325-024-02844-7 – ident: ref_12 doi: 10.3390/cancers14194751 – volume: 7 start-page: 311 year: 2021 ident: ref_24 article-title: Practical Considerations for Optimising Homologous Recombination Repair Mutation Testing in Patients with Metastatic Prostate Cancer publication-title: J. Pathol. Clin. Res. doi: 10.1002/cjp2.203 – ident: ref_2 doi: 10.3390/diagnostics13213350 – volume: 27 start-page: 89 year: 2024 ident: ref_13 article-title: The Impact of Locoregional Treatments for Metastatic Castration Resistant Prostate Cancer on Disease Progression: Real Life Experience from a Multicenter Cohort publication-title: Prostate Cancer Prostatic Dis. doi: 10.1038/s41391-022-00623-5 |
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| Snippet | Background: Approximately 25.0% of metastatic prostate cancer patients harbour DNA damage repair mutations, including BRCA1 and BRCA2, which are actionable... Approximately 25.0% of metastatic prostate cancer patients harbour DNA damage repair mutations, including and , which are actionable targets for... Timely detection of BRCA1/2 mutations is essential for identifying metastatic prostate cancer patients who may benefit from PARP inhibitor therapy. However,... Approximately 25.0% of metastatic prostate cancer patients harbour DNA damage repair mutations, including BRCA1 and BRCA2, which are actionable targets for... |
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| SubjectTerms | Biopsy BRCA1 protein BRCA2 protein Breast cancer Cancer Care and treatment Chi-square test DNA DNA damage DNA fragmentation DNA repair Genetic aspects Health aspects Metastases Metastasis Mutation Next-generation sequencing Poly(ADP-ribose) Poly(ADP-ribose) polymerase Prostate cancer Regression analysis Success |
| Title | Storage Time and DNA Quality Determine BRCA1/2 Sequencing Success in Prostate Cancer: A Multicentre Analysis with Therapeutic Implications |
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