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Association of Germline BRCA2 Mutations with The Letters Benjamin J. Resio, MD BRCA2 as a potential predisposition gene for pediatric or ado- Jessica R. Hoag, PhD lescent lymphoma, we analyzed 794 additional survivors of Alexander S. Chiu, MD lymphoma from the SJLIFE study2 and Childhood Cancer Sur- Andres Monsalve, MD vivor Study3 cohorts, using whole-genome sequencing data. Tejas Sathe, BS Xiao Xu, PhD Methods | Participants included 5-year survivors of pediatric or Daniel J. Boffa, MD adolescent lymphomas. Germline whole-genome sequenc- ing (30-fold coverage) was performed using DNA extracted Author Affiliations: Section of Thoracic Surgery, Department of Surgery, Yale from peripheral blood (SJLIFE study) or buccal or saliva School of Medicine, New Haven, Connecticut (Resio, Hoag, Chiu, Monsalve, samples (Childhood Cancer Survivor Study). This present study Boffa); Yale School of Medicine, New Haven, Connecticut (Sathe); Yale Center for Outcomes Research and Evaluation, New Haven, Connecticut (Xu). was approved by the institutional review board of St Jude Chil- Accepted for Publication: April 14, 2019. dren’s Research Hospital. Study participants provided writ- Published Online: July 11, 2019. doi:10.1001/jamaoncol.2019.1808 ten informed consent at the time of sample collection. Correction: This article was corrected on September 12, 2019, to fix errors in Germline single-nucleotide variants and small insertions the Results section and Table. In the first sentence of the Results section, the and deletions were detected by whole-genome sequencing.4 number of patients should be 73 680 not 2729. The P value for the last row of Genetic variants were annotated, and pathogenicity was clas- the Table (ie, All procedures) should be .06 not .10. sified according to the American College of Medical Genetics Corresponding Author: Daniel J. Boffa, MD, Section of Thoracic Surgery, and Genomics guidelines,5 with the processing pipeline pre- Department of Surgery, Yale School of Medicine, 330 Cedar St. BB205, PO Box 1 208062, New Haven, CT 06520-8062 ([email protected]). viously used in the SJLIFE study cohort. Author Contributions: Drs Resio, Hoag, and Boffa had full access to all of the We downloaded 177 putative loss-of-function BRCA2 mu- data in the study and takes responsibility for the integrity of the data and the tations (excluding those with low confidence), which passed accuracy of the data analysis. quality controls from the whole-exome sequencing source, Study concept and design: Resio, Chiu, Boffa. from gnomAD (Genome Aggregation Database) noncancer set, Acquisition, analysis, or interpretation of data: Resio, Hoag, Chiu, Monsalve, Sathe, Xu. version 2.1. The final numbers of BRCA2 mutation carriers and Drafting of the manuscript: Resio, Boffa. noncarriers were scaled according to the proportion of 3-way Critical revision of the manuscript for important intellectual content: All authors. admixture coefficients of the study population (data from Afri- Statistical analysis: Resio, Hoag, Chiu, Sathe. Obtained funding: Boffa. can, East Asian, and white participants in the 1000 Genomes Administrative, technical, or material support: Resio, Hoag. Project were used as references). Study supervision: Hoag, Boffa. The lymphoma-mutation associations were quantified as Conflict of Interest Disclosures: Dr Xu reported other from Centers for odds ratios (ORs), and their statistical significance was evaluated Medicare & Medicaid Services outside the submitted work. Dr Boffa reported by Fisher exact test. Statistical significance was defined by a nonfinancial support from Epic Sciences outside the submitted work. No other disclosures were reported. 2-sided P = .05. Age-distribution differences were assessed by 1. Gombeski WR Jr, Claypool JO, Karpf M, et al. Hospital affiliations, Wilcoxon rank sum test. R software, version 3.5.2 (R Foundation co-branding, and consumer impact. Health Mark Q. 2014;31(1):65-77. doi:10. for Statistical Computing), was used for statistical analysis. 1080/07359683.2014.874873 2. Chiu AS, Resio B, Hoag JR, et al. US public perceptions about cancer care Results | The 1380 total survivors comprised 815 survivors of provided by smaller hospitals associated with large hospitals recognized for Hodgkin lymphoma and 565 survivors of non–Hodgkin lym- specializing in cancer care. JAMA Oncol. 2018;4(7):1008-1009. doi:10.1001/ jamaoncol.2018.1400 phoma; of whom, 748 (54.2%) were male, and the median 3. Chiu AS, Resio B, Hoag JR, et al. Why travel for complex cancer surgery? (range) age at diagnosis was 13.4 (1.1–22.7) years (Table 1). Most Americans react to ‘brand-sharing’ between specialty cancer hospitals and their participants were white (604 [81.0%] in the SJLIFE study and affiliates. Ann Surg Oncol. 2019;26(3):732-738. doi:10.1245/s10434-018-6868-9 533 [84.1%] in the Childhood Cancer Survivor Study) and had 4. Hoag JR, Resio BJ, Monsalve AF, et al. Differential safety between a similar median (range) age at lymphoma diagnosis (13.5 [1.1- top-ranked cancer hospitals and their affiliates for complex cancer surgery. 22.7] years and 13.3 [1.2-21.0] years). We identified 13 P/LP JAMA Netw Open. 2019;2(4):e191912. doi:10.1001/jamanetworkopen.2019.1912 (pathogenic or likely pathogenic) mutations in BRCA2 (5 mu- 5. Birkmeyer JDSY, Sun Y, Wong SL, Stukel TA. Hospital volume and late survival after cancer surgery. Ann Surg. 2007;245(5):777-783. doi:10.1097/01.sla. tations [0.6%] in survivors of Hodgkin lymphoma, and 8 0000252402.33814.dd mutations [1.4%] in survivors of non–Hodgkin lymphoma). Mu- 6. Sheetz KH, Ryan AM, Ibrahim AM, Dimick JB. Association of hospital tation carriers were indistinguishable from noncarriers on the network participation with surgical outcomes and Medicare expenditures. Ann basis of median (range) age at lymphoma diagnosis (12.8 [6.0- Surg. 2018;(April). doi:10.1097/SLA.0000000000002791 17.7] years vs 13.5 [1.1-22.7] years; P = .40). All 8 survivors of non–Hodgkin lymphoma with BRCA2 mutations were male. Association of Germline BRCA2 Mutations In a comparison with controls without cancer from the With the Risk of Pediatric or Adolescent gnomAD (Table 2), we found a statistically significant asso- Non–Hodgkin Lymphoma ciation between lymphoma and mutations in BRCA2 (OR, 3.3; In a previous report from the St Jude Lifetime (SJLIFE) study, 95% CI, 1.7-5.8). When stratified by diagnosis, the association BRCA2 (GenBank U43746.1) was the third most frequently mu- was statistically significant for non–Hodgkin lymphoma (OR, tated gene (14 occurrences) among 3006 survivors of child- 5.0; 95% CI, 2.1-10.2) but did not achieve statistical signifi- hood cancer, with the highest number observed among sur- cance for Hodgkin lymphoma (OR, 2.1; 95% CI, 0.7-5.1). A ge- vivors of lymphoma (7 [1.2%] of 586).1 To further investigate netic counselor obtained cancer-focused family histories for 1362 JAMA Oncology September 2019 Volume 5, Number 9 (Reprinted) jamaoncology.com © 2019 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 Letters Table 1. Characteristics of the Study Population Survivors of Pediatric or Adolescent Lymphoma, No. (%) Hodgkin Lymphoma Non–Hodgkin Lymphoma All Lymphomas Variable SJLIFE CCSS SJLIFE CCSS SJLIFE CCSS Combined No. of survivors 467 348 279 286 746 634 1380 Sex Male 251 (53.8) 148 (42.5) 182 (65.2) 167 (58.4) 433 (58.0) 315 (49.7) 748 (54.2) Female 216 (46.2) 200 (57.5) 97 (34.8) 119 (41.6) 313 (42.0) 319 (50.3) 632 (45.8) Race/ethnicity White, non-Hispanic 380 (81.4) 298 (85.6) 224 (80.3) 235 (82.2) 604 (81.0) 533 (84.1) 1137 (82.39) Black, non-Hispanic 73 (15.6) 8 (2.3) 47 (16.9) 9 (3.2) 120 (16.1) 17 (2.7) 137 (9.9) Hispanic 8 (1.7) 33 (9.5) 2 (0.72) 18 (6.3) 10 (1.3) 51 (8.0) 61 (4.4) Other/unknown 6 (1.3) 9 (2.6) 6 (2.2) 24 (8.4) 12 (1.6) 33 (5.2) 45 (3.3) Age at primary diagnosis, y 0-4 11 (2.4) 4 (1.2) 38 (13.6) 48 (16.8) 49 (6.6) 52 (8.2) 101 (7.3) 5-9 70 (15.0) 45 (12.9) 93 (33.3) 75 (26.2) 163 (21.9) 120 (18.9) 283 (20.5) 10-14 168 (36.0) 148 (42.5) 89 (31.9) 96 (33.6) 257 (34.5) 244 (38.5) 501 (36.3) ≥15 218 (46.7) 151 (43.4) 59 (21.2) 67 (23.4) 277 (37.1) 218 (34.4) 495 (35.9) Median (range) 14.6 (3.0-22.7) 14.4 (2.0-21.0) 10.3 (1.1-19.9) 11 (1.2-20.9) 13.5 (1.1-22.7) 13.3 (1.2-21.0) 13.4 (1.1-22.7) Abbreviations: CCSS, Childhood Cancer Survivor Study3; SJLIFE, St Jude Lifetime Cohort Study.2 Table 2. Comparison of Cancer Risk Associated With BRCA2 Mutations Among Survivors and Controls No. Lymphoma Survivors Controls From gnomAD Cancer Riska Lymphoma Diagnosis Carriers Noncarriers Carriers Noncarriers OR (95% CI) P Value Hodgkin lymphoma and non–Hodgkin lymphoma 13 1367 170 59 175 3.3 (1.7-5.8) <.001 Hodgkin lymphoma 5 810 169 58 681 2.1 (0.7-5.1) .09 Non–Hodgkin lymphoma 8 557 171 59 902 5.0 (2.1-10.2) <.001 Abbreviations: gnomAD, Genome Aggregation Database; OR, odds ratio. a Cancer risk was calculated by Fisher exact test. 7 of the 8 survivors of non–Hodgkin lymphoma carrying a P/LP non–Hodgkin lymphoma and the penetrance within mutation- BRCA2 mutation. Six survivors had family histories of can- positive individuals will determine whether these recommen- cers, including breast, prostate, pancreas, and melanoma, all dations should be extended to all pediatric or adolescent pa- within the BRCA2-associated cancer spectrum.
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