Cascade testing in Italian Hereditary Breast Ovarian Cancer families: a missed opportunity for cancer prevention?

BRCA1/2 Cascade testing uptake Degree of relationship HBOC Pathogenic variant

Journal

Familial cancer
ISSN: 1573-7292
Titre abrégé: Fam Cancer
Pays: Netherlands
ID NLM: 100898211

Informations de publication

Date de publication:
16 Nov 2023
Historique:
received: 09 07 2023
accepted: 24 10 2023
medline: 16 11 2023
pubmed: 16 11 2023
entrez: 16 11 2023
Statut: aheadofprint

Résumé

Healthy carriers of BRCA1/2 pathogenic variants (PVs) may benefit from risk-reducing measures of proven efficacy. The main approach to identify these individuals is cascade testing, and strategies to support this complex process are under investigation. In Italy, cascade testing has received little attention; therefore, we analyzed the uptake and characteristics of BRCA1/2 cascade testing in families diagnosed with HBOC between 2017 and 2019 at two Italian genetics centers. All blood relatives aged 18 years or older at September 2022 and who could be involved in the first step of cascade testing (i.e., all the living relatives closest to the proband) were included. In addition to first-degree relatives, individuals who were second-, third- or fourth-degree relatives were included if the closest relative(s) was/were deceased. Overall, 213 families were included (103, Genoa; 110, Bologna). Most probands were women affected by breast and/or ovarian cancer (86.4%, Genoa; 84.5%, Bologna), and the branch segregating the PV was known/suspected in 62% of families (62.1%, Genoa; 60.9%, Bologna). Overall, the uptake of cascade testing was 22.8% (25.8%, Genoa; 19.9%, Bologna; OR = 0.59: 95%CI 0.43-0.82). It was strongly associated with female gender (OR = 3.31, 95%CI 2.38-4.59), age ≤ 70 years (< 30 years OR = 3.48, 95%CI 1.85-6.56; 30-70 years OR = 3.08, 95%CI 2.01-4.71), first-degree relationship with the proband (OR = 16.61, 95%CI 10.50-26.28) and segregation of the PV in both the maternal (OR = 2.54, 95%CI 1.72-3.75) and the paternal branch (OR = 4.62, 95%CI 3.09-6.91). These real-world data may be important to inform the design and implementation of strategies aimed at improving the uptake of HBOC cascade testing in Italy.

Identifiants

pubmed: 37968543
doi: 10.1007/s10689-023-00349-w
pii: 10.1007/s10689-023-00349-w
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Yoshida R (2021) Hereditary breast and Ovarian cancer (HBOC): review of its molecular characteristics, screening, treatment, and prognosis. Breast Cancer 28:1167–1180. https://doi.org/10.1007/s12282-020-01148-2
doi: 10.1007/s12282-020-01148-2 pubmed: 32862296
Kuchenbaecker KB, Hopper JL, Barnes DR et al (2017) Risks of breast, ovarian, and contralateral Breast Cancer for BRCA1 and BRCA2 mutation carriers. JAMA 317:2402. https://doi.org/10.1001/jama.2017.7112
doi: 10.1001/jama.2017.7112 pubmed: 28632866
Giri VN, Knudsen KE, Kelly WK et al (2020) Implementation of germline testing for Prostate Cancer: Philadelphia Prostate Cancer Consensus Conference 2019. J Clin Oncol 38:2798–2811. https://doi.org/10.1200/JCO.20.00046
doi: 10.1200/JCO.20.00046 pubmed: 32516092 pmcid: 7430215
Page EC, Bancroft EK, Brook MN et al (2019) Interim results from the IMPACT Study: evidence for prostate-specific Antigen Screening in BRCA2 mutation carriers. Eur Urol 76:831–842. https://doi.org/10.1016/j.eururo.2019.08.019
doi: 10.1016/j.eururo.2019.08.019 pubmed: 31537406 pmcid: 6880781
NCCN Guidelines: Genetic/Familial High-Risk Assessment: Breast, Ovarian, and Pancreatic (Version 1.2024)
King M-C, Levy-Lahad E, Lahad A (2014) Population-based screening for BRCA1 and BRCA2: 2014 Lasker Award. JAMA 312:1091–1092. https://doi.org/10.1001/jama.2014.12483
doi: 10.1001/jama.2014.12483 pubmed: 25198398
Guzauskas GF, Garbett S, Zhou Z et al (2023) Population genomic screening for three Common Hereditary conditions: a cost-effectiveness analysis. Ann Intern Med 176:585–595. https://doi.org/10.7326/M22-0846
doi: 10.7326/M22-0846 pubmed: 37155986
Offit K, Tkachuk KA, Stadler ZK et al (2020) Cascading after Peridiagnostic Cancer Genetic Testing: an alternative to Population-based screening. J Clin Oncol 38:1398–1408. https://doi.org/10.1200/JCO.19.02010
doi: 10.1200/JCO.19.02010 pubmed: 31922925 pmcid: 7193752
Kurian AW, Katz SJ (2020) Emerging opportunity of Cascade Genetic Testing for Population-wide Cancer Prevention and Control. J Clin Oncol 38:1371–1374. https://doi.org/10.1200/JCO.20.00140
doi: 10.1200/JCO.20.00140 pubmed: 32097078
Forbes C, Fayter D, de Kock S, Quek RG (2019) A systematic review of international guidelines and recommendations for the genetic screening, diagnosis, genetic counseling, and treatment of BRCA-mutated Breast cancer. Cancer Manag Res 11:2321–2337. https://doi.org/10.2147/CMAR.S189627
doi: 10.2147/CMAR.S189627 pubmed: 30962720 pmcid: 6434912
Sessa C, Balmaña J, Bober SL et al (2023) Risk reduction and screening of cancer in hereditary breast-ovarian cancer syndromes: ESMO Clinical Practice Guideline. Ann Oncol 34:33–47. https://doi.org/10.1016/j.annonc.2022.10.004
doi: 10.1016/j.annonc.2022.10.004 pubmed: 36307055
Frey MK, Ahsan MD, Bergeron H et al (2022) Cascade Testing for Hereditary Cancer syndromes: should we move toward direct relative contact? A systematic review and Meta-analysis. J Clin Oncol 40:4129–4143. https://doi.org/10.1200/JCO.22.00303
doi: 10.1200/JCO.22.00303 pubmed: 35960887
Whitaker KD, Obeid E, Daly MB, Hall MJ (2021) Cascade Genetic Testing for Hereditary Cancer Risk: An Underutilized Tool for Cancer Prevention. JCO Precis Oncol 5:1387–1396. https://doi.org/10.1200/PO.21.00163
doi: 10.1200/PO.21.00163 pubmed: 34994636
Menko FH, Aalfs CM, Henneman L et al (2013) Informing family members of individuals with Lynch syndrome: a guideline for clinical geneticists. Fam Cancer 12:319–324. https://doi.org/10.1007/s10689-013-9636-9
doi: 10.1007/s10689-013-9636-9 pubmed: 23535968
Di Pietro ML, Zaçe D, Orfino A et al (2021) Intrafamilial communication of hereditary breast and Ovarian cancer genetic information in Italian women: towards a personalised approach. Eur J Hum Genet 29:250–261. https://doi.org/10.1038/s41431-020-00723-7
doi: 10.1038/s41431-020-00723-7 pubmed: 32929237
Ongaro G, Petrocchi S, Calvello M et al (2022) Psychological determinants of men’s adherence to Cascade Screening for BRCA1/2. Curr Oncol 29:2490–2503. https://doi.org/10.3390/curroncol29040203
doi: 10.3390/curroncol29040203 pubmed: 35448177 pmcid: 9030516
Cortesi L, Baldassarri B, Ferretti S et al (2020) A regional population-based hereditary Breast cancer screening tool in Italy: first 5-year results. Cancer Med 9:2579–2589. https://doi.org/10.1002/cam4.2824
doi: 10.1002/cam4.2824 pubmed: 32045136 pmcid: 7131858
Godino L, Turchetti D, Jackson L et al (2019) Presymptomatic genetic testing for hereditary cancer in young adults: a survey of young adults and parents. Eur J Hum Genet 27:291–299. https://doi.org/10.1038/s41431-018-0262-8
doi: 10.1038/s41431-018-0262-8 pubmed: 30287899
Cody N, Green A, McDevitt T, Lynch SA (2008) Cascade screening in BRCA1/2 mutation carriers. Ir Med J 101:140–142
pubmed: 18624259
Jeong GW, Shin W, Lee DO et al (2021) Uptake of family-specific mutation genetic testing among relatives of patients with Ovarian Cancer with BRCA1 or BRCA2 mutation. Cancer Res Treat 53:207–211. https://doi.org/10.4143/crt.2020.364
doi: 10.4143/crt.2020.364 pubmed: 32777875
Julian-Reynier C, Sobol H, Sévilla C et al (2000) Uptake of hereditary breast/ovarian cancer genetic testing in a French national sample of BRCA1 families. The French Cancer Genetic Network. Psychooncology 9:504–510. https://doi.org/10.1002/1099-1611(200011/12)9:6<504::aid-pon491>3.0.co;2-r
doi: 10.1002/1099-1611(200011/12)9:6<504::aid-pon491>3.0.co;2-r pubmed: 11180585
Sanz J, Ramón y Cajal T, Torres A et al (2010) Uptake of predictive testing among relatives of BRCA1 and BRCA2 families: a multicenter study in northeastern Spain. Fam Cancer 9:297–304. https://doi.org/10.1007/s10689-009-9313-1
doi: 10.1007/s10689-009-9313-1 pubmed: 20091130
Lieberman S, Lahad A, Tomer A et al (2018) Familial communication and cascade testing among relatives of BRCA population screening participants. Genet Med 20:1446–1454. https://doi.org/10.1038/gim.2018.26
doi: 10.1038/gim.2018.26 pubmed: 29595811
Gauna Cristaldo FB, Touzani R, Apostolidis T et al (2019) Uptake of genetic counseling among adult children of BRCA1/2 mutation carriers in France. Psychooncology 28:1894–1900. https://doi.org/10.1002/pon.5169
doi: 10.1002/pon.5169 pubmed: 31276266
Hesse-Biber S, Dwyer AA, Yi S (2020) Parent of origin differences in psychosocial burden and approach to BRCA risk management. Breast J 26:734–738. https://doi.org/10.1111/tbj.13633
doi: 10.1111/tbj.13633 pubmed: 31659791
Dwyer AA, Hesse-Biber S, Flynn B, Remick S (2020) Parent of Origin effects on Family Communication of risk in BRCA + women: a qualitative investigation of human factors in Cascade Screening. Cancers (Basel) 12:2316. https://doi.org/10.3390/cancers12082316
doi: 10.3390/cancers12082316 pubmed: 32824510
Finlay E, Stopfer JE, Burlingame E et al (2008) Factors determining dissemination of results and uptake of genetic testing in families with known BRCA1/2 mutations. Genet Test 12:81–91. https://doi.org/10.1089/gte.2007.0037
doi: 10.1089/gte.2007.0037 pubmed: 18373407 pmcid: 3072893
Godino L, Jackson L, Turchetti D et al (2018) Decision making and experiences of young adults undergoing presymptomatic genetic testing for familial cancer: a longitudinal grounded theory study. Eur J Hum Genet 26:44–53. https://doi.org/10.1038/s41431-017-0030-1
doi: 10.1038/s41431-017-0030-1 pubmed: 29162934
Battistuzzi L, Franiuk M, Kasparian N et al (2019) A qualitative study on decision-making about BRCA1/2 testing in Italian women. Eur J Cancer Care (Engl) 28:e13083. https://doi.org/10.1111/ecc.13083
doi: 10.1111/ecc.13083 pubmed: 31056822
Pedrazzani C, Aceti M, Schweighoffer R et al (2022) The communication chain of genetic risk: analyses of Narrative Data Exploring Proband-Provider and Proband-Family Communication in Hereditary breast and Ovarian Cancer. J Pers Med 12:1249. https://doi.org/10.3390/jpm12081249
doi: 10.3390/jpm12081249 pubmed: 36013197 pmcid: 9409642
Sarki M, Ming C, Aceti M et al (2022) Relatives from Hereditary breast and Ovarian Cancer and Lynch Syndrome families forgoing genetic testing: findings from the Swiss CASCADE cohort. J Pers Med 12:1740. https://doi.org/10.3390/jpm12101740
doi: 10.3390/jpm12101740 pubmed: 36294879 pmcid: 9605198
Sarki M, Ming C, Aissaoui S et al (2022) Intention to inform relatives, Rates of Cascade Testing, and preference for patient-mediated communication in families concerned with Hereditary breast and Ovarian Cancer and Lynch Syndrome: the Swiss CASCADE cohort. Cancers (Basel) 14:1636. https://doi.org/10.3390/cancers14071636
doi: 10.3390/cancers14071636 pubmed: 35406409
Menko FH, van der Velden SL, Griffioen DN et al (2023) Does a proactive procedure lead to a higher uptake of predictive testing in families with a pathogenic BRCA1/BRCA2 variant? A family cancer clinic evaluation. J Genet Couns. https://doi.org/10.1002/jgc4.1767
doi: 10.1002/jgc4.1767 pubmed: 37605508

Auteurs

Lucia Trevisan (L)

Unit of Hereditary Cancer, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Lea Godino (L)

Unit of Medical Genetics, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, Italy.

Linda Battistuzzi (L)

Unit of Hereditary Cancer, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Giovanni Innella (G)

Unit of Medical Genetics, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, Italy.
Dipartimento di Scienze Mediche e Chirurgiche, Università di Bologna, Bologna, Italy.

Elena Luppi (E)

Unit of Medical Genetics, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, Italy.
Dipartimento di Scienze Mediche e Chirurgiche, Università di Bologna, Bologna, Italy.

Giulia Buzzatti (G)

Unit of Hereditary Cancer, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Viviana Gismondi (V)

Unit of Hereditary Cancer, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Eva Blondeaux (E)

U.O. Epidemiologia Clinica, IRCCS Ospedale Policlinico San Martino, Largo Rosanna Benzi 10, Genova, 16132, Italy. evablondeaux@gmail.com.

Luigina Ada Bonelli (LA)

U.O. Epidemiologia Clinica, IRCCS Ospedale Policlinico San Martino, Largo Rosanna Benzi 10, Genova, 16132, Italy.

Daniela Turchetti (D)

Unit of Medical Genetics, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, Italy.
Dipartimento di Scienze Mediche e Chirurgiche, Università di Bologna, Bologna, Italy.

Liliana Varesco (L)

Unit of Hereditary Cancer, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Classifications MeSH