The University of Southampton
University of Southampton Institutional Repository

Copy number variants are ovarian cancer risk alleles at known and novel risk loci

Copy number variants are ovarian cancer risk alleles at known and novel risk loci
Copy number variants are ovarian cancer risk alleles at known and novel risk loci

Background: Known risk alleles for epithelial ovarian cancer (EOC) account for approximately 40% of the heritability for EOC. Copy number variants (CNVs) have not been investigated as EOC risk alleles in a large population cohort. Methods: Single nucleotide polymorphism array data from 13071 EOC cases and 17306 controls of White European ancestry were used to identify CNVs associated with EOC risk using a rare admixture maximum likelihood test for gene burden and a by-probe ratio test. We performed enrichment analysis of CNVs at known EOC risk loci and functional biofeatures in ovarian cancer-related cell types. Results: We identified statistically significant risk associations with CNVs at known EOC risk genes; BRCA1 (PEOC = 1.60E-21; OREOC = 8.24), RAD51C (Phigh-grade serous ovarian cancer [HGSOC] = 5.5E-4; odds ratio [OR]HGSOC = 5.74 del), and BRCA2 (PHGSOC = 7.0E-4; ORHGSOC = 3.31 deletion). Four suggestive associations (P <. 001) were identified for rare CNVs. Risk-associated CNVs were enriched (P <. 05) at known EOC risk loci identified by genome-wide association study. Noncoding CNVs were enriched in active promoters and insulators in EOC-related cell types. Conclusions: CNVs in BRCA1 have been previously reported in smaller studies, but their observed frequency in this large population-based cohort, along with the CNVs observed at BRCA2 and RAD51C gene loci in EOC cases, suggests that these CNVs are potentially pathogenic and may contribute to the spectrum of disease-causing mutations in these genes. CNVs are likely to occur in a wider set of susceptibility regions, with potential implications for clinical genetic testing and disease prevention.

0027-8874
1533-1544
Devries, Amber A.
a927623a-4c49-4ee3-b492-282d6b47de21
Dennis, Joe
8fd91fba-10f0-46bf-a98a-2ca796972f56
Tyrer, Jonathan P.
ce04fc42-c1de-4769-841d-f0758f4c973c
Peng, Pei Chen
15ae4038-e7cb-41c9-a299-1b4f1e896235
Coetzee, Simon G.
02576641-a537-46f1-b79d-939e94a35a5c
Reyes, Alberto L.
07d508c9-0ef6-43ed-b980-375850bf8761
Plummer, Jasmine T.
0a2ce6aa-77ca-4247-b7ce-fade57261d71
Davis, Brian D.
b7c52f9f-8ef2-4b3a-a3df-1451b5f3b4e3
Chen, Stephanie S.
8dc1a80e-d57e-44bd-9a62-2d4c7f437547
Dezem, Felipe Segato
2aa6d743-67f4-496b-9c68-afdf206bbf9e
Aben, Katja K.H.
3ef27d47-1dc2-4ad3-b7a2-bf1aece544d7
Anton-Culver, Hoda
a7208921-ed15-4edd-a09b-0e8fb99bc6f6
Antonenkova, Natalia N.
a225af26-6132-4c47-8424-a1dfda09cfc6
Beckmann, Matthias W.
031fc60a-ed4e-4708-995a-12060f501937
Beeghly-Fadiel, Alicia
d0355d79-a847-41fd-90b5-ddf0879f4b72
Berchuck, Andrew
1e234fbd-4421-49d8-9fbf-b19098d71434
Bogdanova, Natalia V.
01efb8fc-f196-4f96-b9e5-cfe4771db721
Bogdanova-Markov, Nadja
c9200d79-13f2-4533-8457-932283537b63
Brenton, James D.
834c3a0f-a453-4de5-908d-c5c21f1533af
Butzow, Ralf
77e849a3-7e63-423f-bc1a-7bf95b2028d1
Campbell, Ian
36052526-40e7-4192-a2d5-15da1b97c4f6
Chang-Claude, Jenny
934a9778-dd8c-4f11-8b14-4d88224bf0c7
Chenevix-Trench, Georgia
27546f1e-7ee5-474f-b9a5-debd27c174d5
Cook, Linda S.
6224555d-9dec-480a-9169-18efac60db4e
Defazio, Anna
3a9c3643-0572-4a28-a233-600ad5867d74
Doherty, Jennifer A.
a31196c0-a68d-4078-ba15-03fb907f81a1
Dork, Thilo
83d24239-fdde-4472-8644-6d9023c802f1
Eccles, Diana M.
5b59bc73-11c9-4cf0-a9d5-7a8e523eee23
Eliassen, A. Heather
6ab6899f-fc52-443d-afe3-2b7cb92443f3
Fasching, Peter A.
a45b84bf-6dfe-41c4-8ea9-f25e65d94d61
Fortner, Renee T.
ee8a43b2-a2f2-4260-be3a-a2dce82944ed
Giles, Graham G.
e0cc73eb-c8eb-450b-b566-fc05e0d2dee3
Goode, Ellen L.
0899e330-6cd5-4196-96f3-ac3a034de1a1
Goodman, Marc T.
2866505e-673c-4af2-a723-30df00d6b893
Gronwald, Jacek
cbd42e84-8d15-4801-a793-6e50dec99c60
Hakansson, Niclas
ddd04c6f-a83f-4d62-a218-6a8c8021e848
Hildebrandt, Michelle A.T.
6f596824-8f45-40d1-922d-889cc938a5f5
Huff, Chad
27182b09-f458-4a63-a0f0-1f7099d79804
Huntsman, David G.
c6c80374-9f3f-41d4-8363-288660bf7cc8
Jensen, Allan
3363733f-fb36-403f-be87-2b5b56fef718
Kar, Siddhartha
647d41fb-d5e7-4af0-b82f-377c92c6691e
Karlan, Beth Y.
15ca2abb-8911-484e-8d06-c6264572b720
Khusnutdinova, Elza K.
610ec330-e0f6-4c0e-96e4-0a8d955d9b0a
Kiemeney, Lambertus A.
414f37d3-8d63-4e8a-8ab7-8b68364b4f14
Kjaer, Susanne K.
cbc4dca5-85cf-4f57-a19d-3e47af44e8fc
Kupryjanczyk, Jolanta
709f6ba4-fe84-487e-a09d-14c0c2d0b015
Labrie, Marilyne
2c61a627-bd50-4a2c-b9c7-540275d9b0ab
Lambrechts, Diether
5248cbcf-eb45-4a52-a9fd-fcc5305f3b39
Le, Nhu D.
1c4ada59-0f57-4afc-aeb6-17c7118fc915
Lubinski, Jan
e7a9709c-36b3-44ed-a5e0-675177ca3d51
May, Taymaa
928bd830-83b8-4489-a59c-e9fc38a74af8
Menon, Usha
f0dd65de-11d4-489a-a468-9589bbe43969
Milne, Roger L.
387456b7-771b-4533-85c8-006c67db7e36
Modugno, Francesmary
a234d152-a897-42f8-8ea5-c04081310c3b
Monteiro, Alvaro N.
a12776ac-6fa6-40fe-ab2a-7b1cb66f2f77
Moysich, Kirsten B.
86962415-5112-450e-aa2d-015161e1994c
Odunsi, Kunle
554f7ad6-362f-4ba2-819c-624886800ed0
Olsson, Hakan
f4a7ed42-dddc-4343-be44-b22f17f75599
Pearce, Celeste L.
a2a655c5-7204-48c6-9da1-662b58e9ff9c
Pejovic, Tanja
74afdf27-a8d3-4f63-877e-053cbac1d3d4
Ramus, Susan J.
7bf16fe9-f3a0-4d29-b20a-77551368e019
Riboli, Elio
046d8687-e25b-433a-8d6a-706b0bb8f314
Riggan, Marjorie J.
6039e677-9248-4dd1-95c0-8e9a99993287
Romieu, Isabelle
26369587-98ff-4280-abb5-140e7d462116
Sandler, Dale P.
24d170de-ad5a-4f8a-a312-069a4a24f235
Schildkraut, Joellen M.
d98e5200-b414-4c2b-9ab2-87cea8fbd762
Setiawan, V. Wendy
57910336-5d91-4812-bf33-fbb888c9ff53
Sieh, Weiva
9d5bdd00-daee-4ad2-a93c-cabf9010a00d
Song, Honglin
90088f14-dc56-4280-83e3-71ad1744858d
Sutphen, Rebecca
67234e96-6ed8-4535-9abe-2ed7b8a73da9
Terry, Kathryn L.
8e556197-4722-4043-9f6a-0b45620acfbc
Thompson, Pamela J.
22cf8806-a909-4e76-8a5b-a1f0a274b7f8
Titus, Linda
09402734-8bb6-413d-8e2c-f61759d10e45
Tworoger, Shelley S.
484fc08e-e285-4b53-a9dd-b72495c4e8c1
Van Nieuwenhuysen, Els
0d971e4d-d1b0-4b4e-8836-566a43d6644d
Edwards, Digna Velez
972cd86b-c51d-437a-8a8a-dba8755564aa
Webb, Penelope M.
d4eb9e8b-60e1-4388-abd7-7149015eba65
Wentzensen, Nicolas
43ddba47-f169-466d-b6aa-c2f5a20e9753
Whittemore, Alice S.
8259d264-e7cc-48df-8ae2-1b8880b47b45
Wolk, Alicja
b49ba21f-ee91-4459-b309-38dbf2daefb3
Wu, Anna H.
75a8d7e9-d941-4810-ac16-6130af242ddd
Ziogas, Argyrios
786f0e72-cf35-4301-805e-6128295e4a4f
Freedman, Matthew L.
3290eddc-35b6-41a9-9364-f27b4911461f
Lawrenson, Kate
b1787caf-36bc-4378-a1f3-11545308f6f1
Pharoah, Paul D.P.
247d3a7d-7b0e-4e9a-ab6d-6f0802a82057
Easton, Douglas F.
2661cf5e-8fc6-4f1d-b27a-e60cac8c8819
Gayther, Simon A.
f374816d-5860-4118-9c68-b93413f95594
Jones, Michelle R.
16e77bd8-d08f-4bfb-ae3e-3c7fafeb8211
Devries, Amber A.
a927623a-4c49-4ee3-b492-282d6b47de21
Dennis, Joe
8fd91fba-10f0-46bf-a98a-2ca796972f56
Tyrer, Jonathan P.
ce04fc42-c1de-4769-841d-f0758f4c973c
Peng, Pei Chen
15ae4038-e7cb-41c9-a299-1b4f1e896235
Coetzee, Simon G.
02576641-a537-46f1-b79d-939e94a35a5c
Reyes, Alberto L.
07d508c9-0ef6-43ed-b980-375850bf8761
Plummer, Jasmine T.
0a2ce6aa-77ca-4247-b7ce-fade57261d71
Davis, Brian D.
b7c52f9f-8ef2-4b3a-a3df-1451b5f3b4e3
Chen, Stephanie S.
8dc1a80e-d57e-44bd-9a62-2d4c7f437547
Dezem, Felipe Segato
2aa6d743-67f4-496b-9c68-afdf206bbf9e
Aben, Katja K.H.
3ef27d47-1dc2-4ad3-b7a2-bf1aece544d7
Anton-Culver, Hoda
a7208921-ed15-4edd-a09b-0e8fb99bc6f6
Antonenkova, Natalia N.
a225af26-6132-4c47-8424-a1dfda09cfc6
Beckmann, Matthias W.
031fc60a-ed4e-4708-995a-12060f501937
Beeghly-Fadiel, Alicia
d0355d79-a847-41fd-90b5-ddf0879f4b72
Berchuck, Andrew
1e234fbd-4421-49d8-9fbf-b19098d71434
Bogdanova, Natalia V.
01efb8fc-f196-4f96-b9e5-cfe4771db721
Bogdanova-Markov, Nadja
c9200d79-13f2-4533-8457-932283537b63
Brenton, James D.
834c3a0f-a453-4de5-908d-c5c21f1533af
Butzow, Ralf
77e849a3-7e63-423f-bc1a-7bf95b2028d1
Campbell, Ian
36052526-40e7-4192-a2d5-15da1b97c4f6
Chang-Claude, Jenny
934a9778-dd8c-4f11-8b14-4d88224bf0c7
Chenevix-Trench, Georgia
27546f1e-7ee5-474f-b9a5-debd27c174d5
Cook, Linda S.
6224555d-9dec-480a-9169-18efac60db4e
Defazio, Anna
3a9c3643-0572-4a28-a233-600ad5867d74
Doherty, Jennifer A.
a31196c0-a68d-4078-ba15-03fb907f81a1
Dork, Thilo
83d24239-fdde-4472-8644-6d9023c802f1
Eccles, Diana M.
5b59bc73-11c9-4cf0-a9d5-7a8e523eee23
Eliassen, A. Heather
6ab6899f-fc52-443d-afe3-2b7cb92443f3
Fasching, Peter A.
a45b84bf-6dfe-41c4-8ea9-f25e65d94d61
Fortner, Renee T.
ee8a43b2-a2f2-4260-be3a-a2dce82944ed
Giles, Graham G.
e0cc73eb-c8eb-450b-b566-fc05e0d2dee3
Goode, Ellen L.
0899e330-6cd5-4196-96f3-ac3a034de1a1
Goodman, Marc T.
2866505e-673c-4af2-a723-30df00d6b893
Gronwald, Jacek
cbd42e84-8d15-4801-a793-6e50dec99c60
Hakansson, Niclas
ddd04c6f-a83f-4d62-a218-6a8c8021e848
Hildebrandt, Michelle A.T.
6f596824-8f45-40d1-922d-889cc938a5f5
Huff, Chad
27182b09-f458-4a63-a0f0-1f7099d79804
Huntsman, David G.
c6c80374-9f3f-41d4-8363-288660bf7cc8
Jensen, Allan
3363733f-fb36-403f-be87-2b5b56fef718
Kar, Siddhartha
647d41fb-d5e7-4af0-b82f-377c92c6691e
Karlan, Beth Y.
15ca2abb-8911-484e-8d06-c6264572b720
Khusnutdinova, Elza K.
610ec330-e0f6-4c0e-96e4-0a8d955d9b0a
Kiemeney, Lambertus A.
414f37d3-8d63-4e8a-8ab7-8b68364b4f14
Kjaer, Susanne K.
cbc4dca5-85cf-4f57-a19d-3e47af44e8fc
Kupryjanczyk, Jolanta
709f6ba4-fe84-487e-a09d-14c0c2d0b015
Labrie, Marilyne
2c61a627-bd50-4a2c-b9c7-540275d9b0ab
Lambrechts, Diether
5248cbcf-eb45-4a52-a9fd-fcc5305f3b39
Le, Nhu D.
1c4ada59-0f57-4afc-aeb6-17c7118fc915
Lubinski, Jan
e7a9709c-36b3-44ed-a5e0-675177ca3d51
May, Taymaa
928bd830-83b8-4489-a59c-e9fc38a74af8
Menon, Usha
f0dd65de-11d4-489a-a468-9589bbe43969
Milne, Roger L.
387456b7-771b-4533-85c8-006c67db7e36
Modugno, Francesmary
a234d152-a897-42f8-8ea5-c04081310c3b
Monteiro, Alvaro N.
a12776ac-6fa6-40fe-ab2a-7b1cb66f2f77
Moysich, Kirsten B.
86962415-5112-450e-aa2d-015161e1994c
Odunsi, Kunle
554f7ad6-362f-4ba2-819c-624886800ed0
Olsson, Hakan
f4a7ed42-dddc-4343-be44-b22f17f75599
Pearce, Celeste L.
a2a655c5-7204-48c6-9da1-662b58e9ff9c
Pejovic, Tanja
74afdf27-a8d3-4f63-877e-053cbac1d3d4
Ramus, Susan J.
7bf16fe9-f3a0-4d29-b20a-77551368e019
Riboli, Elio
046d8687-e25b-433a-8d6a-706b0bb8f314
Riggan, Marjorie J.
6039e677-9248-4dd1-95c0-8e9a99993287
Romieu, Isabelle
26369587-98ff-4280-abb5-140e7d462116
Sandler, Dale P.
24d170de-ad5a-4f8a-a312-069a4a24f235
Schildkraut, Joellen M.
d98e5200-b414-4c2b-9ab2-87cea8fbd762
Setiawan, V. Wendy
57910336-5d91-4812-bf33-fbb888c9ff53
Sieh, Weiva
9d5bdd00-daee-4ad2-a93c-cabf9010a00d
Song, Honglin
90088f14-dc56-4280-83e3-71ad1744858d
Sutphen, Rebecca
67234e96-6ed8-4535-9abe-2ed7b8a73da9
Terry, Kathryn L.
8e556197-4722-4043-9f6a-0b45620acfbc
Thompson, Pamela J.
22cf8806-a909-4e76-8a5b-a1f0a274b7f8
Titus, Linda
09402734-8bb6-413d-8e2c-f61759d10e45
Tworoger, Shelley S.
484fc08e-e285-4b53-a9dd-b72495c4e8c1
Van Nieuwenhuysen, Els
0d971e4d-d1b0-4b4e-8836-566a43d6644d
Edwards, Digna Velez
972cd86b-c51d-437a-8a8a-dba8755564aa
Webb, Penelope M.
d4eb9e8b-60e1-4388-abd7-7149015eba65
Wentzensen, Nicolas
43ddba47-f169-466d-b6aa-c2f5a20e9753
Whittemore, Alice S.
8259d264-e7cc-48df-8ae2-1b8880b47b45
Wolk, Alicja
b49ba21f-ee91-4459-b309-38dbf2daefb3
Wu, Anna H.
75a8d7e9-d941-4810-ac16-6130af242ddd
Ziogas, Argyrios
786f0e72-cf35-4301-805e-6128295e4a4f
Freedman, Matthew L.
3290eddc-35b6-41a9-9364-f27b4911461f
Lawrenson, Kate
b1787caf-36bc-4378-a1f3-11545308f6f1
Pharoah, Paul D.P.
247d3a7d-7b0e-4e9a-ab6d-6f0802a82057
Easton, Douglas F.
2661cf5e-8fc6-4f1d-b27a-e60cac8c8819
Gayther, Simon A.
f374816d-5860-4118-9c68-b93413f95594
Jones, Michelle R.
16e77bd8-d08f-4bfb-ae3e-3c7fafeb8211

Devries, Amber A., Dennis, Joe, Tyrer, Jonathan P., Peng, Pei Chen, Coetzee, Simon G., Reyes, Alberto L., Plummer, Jasmine T., Davis, Brian D., Chen, Stephanie S., Dezem, Felipe Segato, Aben, Katja K.H., Anton-Culver, Hoda, Antonenkova, Natalia N., Beckmann, Matthias W., Beeghly-Fadiel, Alicia, Berchuck, Andrew, Bogdanova, Natalia V., Bogdanova-Markov, Nadja, Brenton, James D., Butzow, Ralf, Campbell, Ian, Chang-Claude, Jenny, Chenevix-Trench, Georgia, Cook, Linda S., Defazio, Anna, Doherty, Jennifer A., Dork, Thilo, Eccles, Diana M., Eliassen, A. Heather, Fasching, Peter A., Fortner, Renee T., Giles, Graham G., Goode, Ellen L., Goodman, Marc T., Gronwald, Jacek, Hakansson, Niclas, Hildebrandt, Michelle A.T., Huff, Chad, Huntsman, David G., Jensen, Allan, Kar, Siddhartha, Karlan, Beth Y., Khusnutdinova, Elza K., Kiemeney, Lambertus A., Kjaer, Susanne K., Kupryjanczyk, Jolanta, Labrie, Marilyne, Lambrechts, Diether, Le, Nhu D., Lubinski, Jan, May, Taymaa, Menon, Usha, Milne, Roger L., Modugno, Francesmary, Monteiro, Alvaro N., Moysich, Kirsten B., Odunsi, Kunle, Olsson, Hakan, Pearce, Celeste L., Pejovic, Tanja, Ramus, Susan J., Riboli, Elio, Riggan, Marjorie J., Romieu, Isabelle, Sandler, Dale P., Schildkraut, Joellen M., Setiawan, V. Wendy, Sieh, Weiva, Song, Honglin, Sutphen, Rebecca, Terry, Kathryn L., Thompson, Pamela J., Titus, Linda, Tworoger, Shelley S., Van Nieuwenhuysen, Els, Edwards, Digna Velez, Webb, Penelope M., Wentzensen, Nicolas, Whittemore, Alice S., Wolk, Alicja, Wu, Anna H., Ziogas, Argyrios, Freedman, Matthew L., Lawrenson, Kate, Pharoah, Paul D.P., Easton, Douglas F., Gayther, Simon A. and Jones, Michelle R. (2022) Copy number variants are ovarian cancer risk alleles at known and novel risk loci. Journal of the National Cancer Institute, 114 (11), 1533-1544. (doi:10.1093/jnci/djac160).

Record type: Article

Abstract

Background: Known risk alleles for epithelial ovarian cancer (EOC) account for approximately 40% of the heritability for EOC. Copy number variants (CNVs) have not been investigated as EOC risk alleles in a large population cohort. Methods: Single nucleotide polymorphism array data from 13071 EOC cases and 17306 controls of White European ancestry were used to identify CNVs associated with EOC risk using a rare admixture maximum likelihood test for gene burden and a by-probe ratio test. We performed enrichment analysis of CNVs at known EOC risk loci and functional biofeatures in ovarian cancer-related cell types. Results: We identified statistically significant risk associations with CNVs at known EOC risk genes; BRCA1 (PEOC = 1.60E-21; OREOC = 8.24), RAD51C (Phigh-grade serous ovarian cancer [HGSOC] = 5.5E-4; odds ratio [OR]HGSOC = 5.74 del), and BRCA2 (PHGSOC = 7.0E-4; ORHGSOC = 3.31 deletion). Four suggestive associations (P <. 001) were identified for rare CNVs. Risk-associated CNVs were enriched (P <. 05) at known EOC risk loci identified by genome-wide association study. Noncoding CNVs were enriched in active promoters and insulators in EOC-related cell types. Conclusions: CNVs in BRCA1 have been previously reported in smaller studies, but their observed frequency in this large population-based cohort, along with the CNVs observed at BRCA2 and RAD51C gene loci in EOC cases, suggests that these CNVs are potentially pathogenic and may contribute to the spectrum of disease-causing mutations in these genes. CNVs are likely to occur in a wider set of susceptibility regions, with potential implications for clinical genetic testing and disease prevention.

Text
djac160 - Version of Record
Download (1MB)

More information

Accepted/In Press date: 18 August 2022
Published date: 10 October 2022
Additional Information: Funding: This work was supported by the National Institute of General Medical Sciences of the National Institutes of Health (5T32GM118288-03); the CSMC Precision Health Initiative; and the Tell Every Amazing Lady About Ovarian Cancer Louisa M. McGregor Ovarian Cancer Foundation. Supported in part by the Ovarian Cancer Research Fund thanks to donations by the family and friends of Kathryn Sladek Smith (PPD/RPCI.07); the US National Cancer Institute GAME-ON Post-GWAS Initiative (U19-CA148112); the Wellcome Trust (076113; the National Cancer Institute and National Human Genome Research Institute (dbGap accession number phs000178.v8.p7); the U.S. National Institutes of Health (CA1X01HG007491-01 (CIA), U19-CA148112 (TAS), R01-CA149429 (CMP) and R01-CA058598 (MTG); Canadian Institutes of Health Research (MOP-86727 (LEK); the Ovarian Cancer Research Fund (AB); a European Commission’s Seventh Framework Programme grant (agreement number 223175 - HEALTH-F2-2009-223175); the U.S. Army Medical Research and Materiel Command (DAMD17-01-1-0729); National Health & Medical Research Council of Australia (199600, 400413 and 400281); Cancer Councils of New South Wales, Victoria, Queensland, South Australia and Tasmania and Cancer Foundation of Western Australia (Multi-State Applications 191, 211 and 182); Ovarian Cancer Australia and the Peter MacCallum Foundation; ELAN Funds of the University of Erlangen-Nuremberg; National Kankerplan; Breast Cancer Now, Institute of Cancer Research; the National Institutes of Health (NIH)/National Center for Advancing Translational Sciences (NCATS) (ULTR000445 - the 1S10RR025141-01 instrumentation award and Vanderbilt CTSA grant); the European Commission (DG-SANCO); the International Agency for Research on Cancer; Danish Cancer Society (Denmark) (EMC 2014-6699); Ligue Contre le Cancer, Institut Gustave Roussy, Mutuelle Générale de l’Education Nationale; Institut National de la Santé et de la Recherche Médicale (INSERM) (France); German Cancer Aid; German Cancer Research Center (DKFZ); Federal Ministry of Education and Research (BMBF) (Germany); the Hellenic Health Foundation (Greece); Associazione Italiana per la Ricerca sul Cancro-AIRC-Italy and National Research Council (Italy); Dutch Ministry of Public Health, Welfare and Sports (VWS); Netherlands Cancer Registry (NKR); LK Research Funds; Dutch Prevention Funds; Dutch ZON (Zorg Onderzoek Nederland); World Cancer Research Fund (WCRF); Statistics Netherlands (the Netherlands); ERC-2009-AdG 232997 and Nordforsk, Nordic Centre of Excellence programme on Food, Nutrition and Health (Norway); Health Research Fund (FIS), PI13/00061 to Granada, PI13/01162 to EPIC-Murcia; Regional Governments of Andalucía, Asturias, Basque Country, Murcia and Navarra, ISCIII RETIC (RD06/0020) (Spain); Swedish Cancer Society, Swedish Research Council and County Councils of Skåne and Västerbotten (Sweden); Cancer Research UK (14136 to EPIC-Norfolk; C570/A16491 and C8221/A19170 to EPIC-Oxford), Medical Research Council (1000143 to EPIC-Norfolk, MR/M012190/1 to EPIC-Oxford) (United Kingdom); German Federal Ministry of Education and Research, Programme of Clinical Biomedical Research (01 GB 9401) and the German Cancer Research Center (DKFZ); U.S. National Institutes of Health (R01-CA58598, N01-CN-55424 and N01-PC-67001); intramural funding; Rudolf-Bartling Foundation; Helsinki University Hospital Research Fund; University of Pittsburgh School of Medicine Dean’s Faculty Advancement Award (F. Modugno); Department of Defense (DAMD17-02-1-0669); NCI (K07-CA080668, R01-CA95023, P50-CA159981 MO1-RR000056 R01-CA126841); intramural funding from the Rudolf-Bartling Foundation; ERC-2011-AdG 294576-risk factors cancer, Swedish Cancer Society, Swedish Research Council, Beta Kamprad Foundation; the National Cancer Institute (R01- CA61107), the Danish Cancer Society, Copenhagen, Denmark (94 222 52); the Mermaid I project; National Institutes of Health (R01-CA122443, P30-CA15083, P50-CA136393); Mayo Foundation; Minnesota Ovarian Cancer Alliance; Fred C. and Katherine B. Andersen Foundation; VicHealth and Cancer Council Victoria, Cancer Council Victoria, National Health and Medical Research Council of Australia (NHMRC) (209057, 251533, 396414, and 504715); DOD Ovarian Cancer Research Program (W81XWH-07-0449); Moffitt Cancer Center; Merck Pharmaceuticals; the state of Florida; Hillsborough County; the city of Tampa; National Institutes of Health (R01-CA76016); the Department of Defense (DAMD17-02-1-0666); National Institutes of Health (R01-CA54419 and P50-CA105009); Department of Defense (W81XWH-10-1-02802. UM1 CA186107, P01 CA87969, R01 CA49449, R01-CA67262, UM1 CA176726); Radboud University Medical Centre; Canadian Institutes of Health Research grant (MOP-86727); National Institutes of Health/National Cancer Institute 1 (R01CA160669-01A1); Intramural Research Program of the National Cancer Institute; Pomeranian Medical University; Cancer Research UK (C490/A10119 C490/A10124); UK National Institute for Health Research Biomedical Research Centres at the University of Cambridge; Intramural Research Program of the NIH, National Institute of Environmental Health Sciences (Z01-ES044005 and Z01-ES049033); The Swedish Cancer Foundation and the Swedish Research Council (VR 2017-00644); National Institutes of Health (R01-CA106414-A2); American Cancer Society (CRTG-00-196-01-CCE); Department of Defense (DAMD17-98-1-8659); Celma Mastry Ovarian Cancer Foundation; National Institutes of Health (R01-CA058860); the Lon V Smith Foundation (LVS-39420); The Eve Appeal (The Oak Foundation); National Institute for Health Research University College London Hospitals Biomedical Research Centre and MRC core funding (MR_UU_12023); P01CA17054, P30CA14089, R01CA61132, N01PC67010, R03CA113148, R03CA115195, N01CN025403, and California Cancer Research Program (00-01389 V-20170, 2II0200); National Science Centre (N N301 5645 40); The Maria Sklodowska-Curie Memorial Cancer Centre; and the Institute of Oncology, Warsaw, Poland. The Nurses’ Health Study (NHS) was supported by the National Institutes of Health (UM1 CA186107, P01 CA87969, R01 CA49449) and the NHS II was supported by the National Institutes of Health (U01 CA176726, R01 CA67262). Joe Dennis is supported by the CanRisk Cancer Research UK programme grant: PPRPGM-Nov20\100002 and by the Confluence project which is funded with intramural funds from the National Cancer Institute Intramural Research Programme, National Institutes of Health.

Identifiers

Local EPrints ID: 478022
URI: http://eprints.soton.ac.uk/id/eprint/478022
ISSN: 0027-8874
PURE UUID: acfba11b-bea0-4b01-a09f-ca1b0432f0af
ORCID for Diana M. Eccles: ORCID iD orcid.org/0000-0002-9935-3169

Catalogue record

Date deposited: 19 Jun 2023 17:02
Last modified: 17 Mar 2024 02:36

Export record

Altmetrics

Contributors

Author: Amber A. Devries
Author: Joe Dennis
Author: Jonathan P. Tyrer
Author: Pei Chen Peng
Author: Simon G. Coetzee
Author: Alberto L. Reyes
Author: Jasmine T. Plummer
Author: Brian D. Davis
Author: Stephanie S. Chen
Author: Felipe Segato Dezem
Author: Katja K.H. Aben
Author: Hoda Anton-Culver
Author: Natalia N. Antonenkova
Author: Matthias W. Beckmann
Author: Alicia Beeghly-Fadiel
Author: Andrew Berchuck
Author: Natalia V. Bogdanova
Author: Nadja Bogdanova-Markov
Author: James D. Brenton
Author: Ralf Butzow
Author: Ian Campbell
Author: Jenny Chang-Claude
Author: Georgia Chenevix-Trench
Author: Linda S. Cook
Author: Anna Defazio
Author: Jennifer A. Doherty
Author: Thilo Dork
Author: Diana M. Eccles ORCID iD
Author: A. Heather Eliassen
Author: Peter A. Fasching
Author: Renee T. Fortner
Author: Graham G. Giles
Author: Ellen L. Goode
Author: Marc T. Goodman
Author: Jacek Gronwald
Author: Niclas Hakansson
Author: Michelle A.T. Hildebrandt
Author: Chad Huff
Author: David G. Huntsman
Author: Allan Jensen
Author: Siddhartha Kar
Author: Beth Y. Karlan
Author: Elza K. Khusnutdinova
Author: Lambertus A. Kiemeney
Author: Susanne K. Kjaer
Author: Jolanta Kupryjanczyk
Author: Marilyne Labrie
Author: Diether Lambrechts
Author: Nhu D. Le
Author: Jan Lubinski
Author: Taymaa May
Author: Usha Menon
Author: Roger L. Milne
Author: Francesmary Modugno
Author: Alvaro N. Monteiro
Author: Kirsten B. Moysich
Author: Kunle Odunsi
Author: Hakan Olsson
Author: Celeste L. Pearce
Author: Tanja Pejovic
Author: Susan J. Ramus
Author: Elio Riboli
Author: Marjorie J. Riggan
Author: Isabelle Romieu
Author: Dale P. Sandler
Author: Joellen M. Schildkraut
Author: V. Wendy Setiawan
Author: Weiva Sieh
Author: Honglin Song
Author: Rebecca Sutphen
Author: Kathryn L. Terry
Author: Pamela J. Thompson
Author: Linda Titus
Author: Shelley S. Tworoger
Author: Els Van Nieuwenhuysen
Author: Digna Velez Edwards
Author: Penelope M. Webb
Author: Nicolas Wentzensen
Author: Alice S. Whittemore
Author: Alicja Wolk
Author: Anna H. Wu
Author: Argyrios Ziogas
Author: Matthew L. Freedman
Author: Kate Lawrenson
Author: Paul D.P. Pharoah
Author: Douglas F. Easton
Author: Simon A. Gayther
Author: Michelle R. Jones

Download statistics

Downloads from ePrints over the past year. Other digital versions may also be available to download e.g. from the publisher's website.

View more statistics

Atom RSS 1.0 RSS 2.0

Contact ePrints Soton: eprints@soton.ac.uk

ePrints Soton supports OAI 2.0 with a base URL of http://eprints.soton.ac.uk/cgi/oai2

This repository has been built using EPrints software, developed at the University of Southampton, but available to everyone to use.

We use cookies to ensure that we give you the best experience on our website. If you continue without changing your settings, we will assume that you are happy to receive cookies on the University of Southampton website.

×