Abstract
CDH1 gene mutations have been found to be associated with diffuse type gastric cancer and invasive lobular carcinoma (ILC) of the breast. To the best of our knowledge, this is the only study relating a family history of gastric cancer to ILC of the breast. We conducted a retrospective study comparing the family history of malignancies in patients with invasive ductal carcinoma (IDC) of the breast and ILC treated in our Medical Center. The comparison was evaluated in both types of breast cancer groups, dividing the patients into two age groups, <50 and ≥50 years. One thousand one hundred and sixty-seven patients with IDC and ILC entered the study. A family history of malignancies was reported in 21.6 % of patients with IDC as opposed to 37.8 % of patients with ILC (P < 0.001). A history of gastric cancer was reported in 7.2 % in the ILC group as compared to 2.3 % in the IDC group, P < 0.008. A family history of breast cancer was more common in the ILC group as opposed to the IDC group, 18 versus 8.1 % respectively, P = 0.002 and persisted in both age groups. We conclude that a family history of malignancies in first degree relatives is more common in patients with ILC than IDC and that there is a significant association between a family history of gastric cancer and ILC.
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Keller G, Vogelsang H, Becker I, Hutter J, Ott K, Candidus S, Grundei T, Becker KF, Mueller J, Siewert JR, Höfler H (1999) Diffuse type gastric and lobular breast carcinoma in a familial gastric cancer patient with an E-Cadherin germline mutation. Am J Pathol 155:337–342
Reis-Filho JS, Simpson PT, Jones C, Steele D, Mackay A, Iravani M, Fenwick K, Valgeirsson H, Lambros M, Ashworth A, Palacios J, Schmitt F, Lakhani SR (2005) Pleomorphic lobular carcinoma of the breast: role of comprehensive molecular pathology in characterization of an entity. J Pathol 207:1–13
Masciari S, Larsson N, Senz J, Boyd N, Kaurah P, Kandel MJ, Harris LN, Pinheiro HC, Troussard A, Miron P, Tung N, Oliveira C, Collins L, Schnitt S, Garber JE, Huntsman D (2007) Germline E-cadherin mutations in familial lobular breast cancer. J Med Genet 44:726–731
Brooks-Wilson AR, Kaurah P, Suriano G, Leach S, Senz J, Grehan N, Butterfield YS, Jeyes J, Schinas J, Bacani J, Kelsey M, Ferreira P, MacGillivray B, MacLeod P, Micek M, Ford J, Foulkes W, Australie K, Greenberg C, LaPointe M, Gilpin C, Nikkel S, Gilchrist D, Hughes R, Jackson CE, Monaghan KG, Oliveira MJ, Seruca R, Gallinger S, Caldas C, Huntsman D (2004) Germline E-cadherin mutations in hereditary diffuse gastric cancer: assessment of 42 new families and review of genetic screening criteria. J Med Genet 41:508–517
Schrader KA, Masciari S, Boyd N, Salamanca C, Senz J, Saunders DN, Yorida E, Maines-Bandiera S, Kaurah P, Tung N, Robson ME, Ryan PD, Olopade OI, Domchek SM, Ford J, Isaacs C, Brown P, Balmana J, Razzak AR, Miron P, Coffey K, Terry MB, John EM, Andrulis IL, Knight JA, O’Malley FP, Daly M, Bender P, kConFab, Moore R, Southey MC, Hopper JL, Garber JE, Huntsman DG (2011) Germline mutations in CDH1 are infrequent in women with early-onset or familial lobular breast cancers. J Med Genet 48:64–68
Jonsson BA, Bergh A, Stattin P, Emmanuelsson M, Grönberg H (2002) Germline mutations in E-cadherin do not explain association of hereditary prostate cancer, gastric cancer and breast cancer. Int J Cancer 98:838–843
Kaurah P, MacMillan A, Boyd N, Senz J, De Luca A, Chun N, Suriano G, Zaor S, Van Manen L, Gilpin C, Nikkel S, Connolly-Wilson M, Weissman S, Rubinstein WS, Sebold C, Greenstein R, Stroop J, Yim D, Panzini B, McKinnon W, Greenblatt M, Wirtzfeld D, Fontaine D, Coit D, Yoon S, Chung D, Lauwers G, Pizzuti A, Vaccaro C, Redal MA, Oliveira C, Tischkowitz M, Olschwang S, Gallinger S, Lynch H, Green J, Ford J, Pharoah P, Fernandez B, Huntsman D (2007) Founder and recurrent CDH1 mutations in families with hereditary diffuse gastric cancer. JAMA 297:2360–2372
Hansford S, Pardeep Kaurah P, Li-Chang H, Woo M, Senz J, Pinheiro H, Schrader KA, Schaeffer DF, Shumansky K, Zogopoulos G, Santos TA, Claro I, Carvalho J, Nielsen C, Padilla S, Lum A, Talhouk A, Baker-Lange K, Richardson S, Lewis I, Lindor NM, Pennell E, MacMillan A, Fernandez B, Keller G, Lynch H, Shah SP, Guilford P, Gallinger S, Corso G, Roviello F, Caldas C, Oliveira C, Pharoah PDP, Huntsman DG (2015) Hereditary diffuse gastric cancer syndrome. CDH1 mutations and beyond. JAMA Oncol 1:23–32
van der Post RS, Vogelaar IP, Manders P, van der Kolk LE, Cats A, van Hest LP, Sijmons R, Aalfs CM, Ausems MG, Gómez García EB, Wagner A, Hes FJ, Arts N, Mensenkamp AR, van Krieken JH, Hoogerbrugge N, Ligtenberg MJ (2015) Accuracy of hereditary diffuse gastric cancer testing criteria and outcomes in patients with a germline mutation in CDH1. Gastroenterology. doi:10.1053/j.gastro.2015.06.003
Oliveira C, Pinheiro H, Figueiredo J, Seruca R, Cameiro F (2015) Familial gastric cancer: genetic susceptibility, pathology, and implications for management. Lancet Oncol 16:e60–e70
Li CI, Anderson BO, Daling JR, Moe RE (2003) Trends in incidence rates of invasive lobular and ductal breast carcinoma. JAMA 289:1421–1424
Chikman B, Lavy R, Davidson T, Wassermann I, Sandbank J, Siegelmann-Danieli N, Halevy A (2010) Factors affecting rise in the incidence of infiltrating lobular carcinoma of the breast. IMAJ 12:697–700
Pestalozzi BC, Zahrieh D, Mallon E, Gusterson BA, Price KN, Gelber RD, Holmberg SB, Lindtner J, Snyder R, Thürlimann B, Murray E, Viale G, Castiglione-Gertsch M, Coates AS, Goldhirsch A; International Breast Cancer Study Group (2008) Distinct clinical and prognostic features of infiltrating lobular carcinoma of the breast: combined results of 15 international breast cancer study group clinical trials. J Clin Oncol 26:3006–3014
Arpino G, Bardou VJ, Clark GM, Elledge RM (2004) Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cancer Res 6:R149–R156
Zhao H, LangerØdA Ji Y, Nowels KW, Nesland JM, Tibshirani R, Bukholm IK, Kåresen R, Botstein D, Børresen-Dale AL, Jeffrey SS (2004) Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Mol Biol Cell 15:2523–2536
Dossus L, Benusiglio PR (2015) Lobular breast cancer: incidence and genetic and non-genetic risk factors. Breast Cancer Res 17:37
Collaborative Group on Hormonal Factors in Breast Cancer (2001) Familial breast cancer: collaborative reanalysis of individual data from 52 epidemiological studies including 58,209 women with breast cancer and 101,986 women without the disease. Lancet 358:1389–1399
Colditz GA, Willett WC, Hunter DJ, Stampfer MJ, Manson JE, Hennekens CH, Rosner BA (1993) Family history, age and risk of breast cancer. Prospective data from the Nurses’ Health Study. JAMA 270:338–343
McTiernan A, Kuniyuki A, Yasui Y, Bowen D, Burke W, Culver JB, Anderson R, Durfy S (2001) Comparison of two breast cancer risk estimates in woman with a family history of breast cancer. Cancer Epidemiol Biomarkers Prev 10:333–338
Clark AS, Domchek SM (2011) Clinical management of hereditary breast cancer syndromes. J Mammary Gland Biol Neoplasia 16:17–25
Chen YC, Hunter DJ (2005) Molecular epidemiology of cancer. CA Cancer J Clin 55:45–54
Easton DF, Pharoah PDP, Antoniou AC, Tischkowitz M, Tavtigian SV, Nathanson KL, Devilee P, Meindl A, Couch FJ, Southey M, Goldgar DE, Evans DGR, Chenevix-Trench G, Rahman N, Robson M, Domchek SM, Foulkes WD (2015) Gene-panel sequencing and the prediction of breast-cancer risk. N Engl J Med 372:2243–2257
Hemminki K, Granstrom C (2002) Familial breast carcinoma risks by morphology: a nationwide epidemiologic study from Sweden. Cancer 94:3063–3070
Li CI, Daling JR, Malone KE, Bernstein L, Marchbanks PA, Liff JM, Strom BL, Simon MS, Press MF, McDonald JA, Ursin G, Burkman RT, Deapen D, Spirtas R (2006) Relationship between established breast cancer risk factors and risk of seven different histologic types of invasive breast cancer. Cancer Epidemiol Biomarkers Prev 15:946–954
Lakhani SR, Gusterson BA, Jacquemier J, Sloane JP, Anderson TJ, van de Vijver MJ, Venter D, Freeman A, Antoniou A, McGuffog L, Smyth E, Steel CM, Haites N, Scott RJ, Goldgar D, Neuhausen S, Daly PA, Ormiston W, McManus R, Scherneck S, Ponder BA, Futreal PA, Peto J, Stoppa-Lyonnet D, Bignon YJ, Stratton MR (2000) The pathology of familial breast cancer: histological features of cancers in families not attributable to mutations in BRCA1 or BRCA2. Clin Cancer Res 6:782–789
Fitzgerald RC, Hardwick R, Huntsman D, Carneiro F, Guilford P, Blair V, Chung DC, Norton J, Ragunath K, Van Krieken JH, Dwerryhouse S, Caldas C; International Gastric Cancer Linkage Consortium (2010) Hereditary diffuse gastric cancer: updated consensus guidelines for clinical management and directions for future research. J Med Genet 47:436–444
Benusiglio PR, Malka D, Rouleau E, Buecher B, Nogues C, Fourme E, Colas C, Coulet F, Warcoin M, Grandjouan S, Sezeur A, Laurent-Puig P, Molière D, Tlemsani C, Di Maria M, Byrde V, Delaloge S, Blayau M, Caron O (2013) CDH1 germline mutations and the hereditary gastric and lobular breast cancer syndrome: a multicenter study. J Med Genet 50:486–489
Petridis C, Shinomiya I, Kohut K, Gorman P, Caneppele M, Shah V, Troy M, Pinder SE, Hanby A, Tomlinson I, Trembath RC, Roylance R, Simpson MA, Sawyer EJ (2014) Germline CDH1 mutations in bilateral lobular carcinoma in situ. Br J Cancer 110:1053–1057
Bermejo JL, Hemminki K (2005) A population-based assessment of the clustering of breast cancer in families eligible for testing of BRCA1 and BRCA2 mutations. Ann Oncol 16:322–329
Lonning PE, Knappskog S, Staalesen V, Chrisanthar R, Lillehaug JR (2007) Breast cancer prognostication and prediction in the postgenomic era. Ann Oncol 18:1293–1306
Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406:747–752
Saslow D, Boetes C, Burke W, Harms S, Leach MO, Lehman CD, Morris E, Pisano E, Schnall M, Sener S, Smith RA, Warner E, Yaffe M, Andrews KS, Russell CA; American Cancer Society Breast Cancer Advisory Group (2007) American Cancer Society Breast Society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J Clin 57:75–89
Yang XR, Sherman ME, Rimm DL, Lissowska J, Brinton LA, Peplonska B, Hewitt SM, Anderson WF, Szeszenia-Dabrowska N, Bardin-Mikolajczak A, Zatonski W, Cartun R, Mandich D, Rymkiewicz G, Ligaj M, Lukaszek S, Kordek R, García-Closas M (2007) Differences in risk factors for breast cancer molecular subtypes in a population-based Study. Cancer Epidemiol Biomarkers Prev 16:439–443
Couto E, Banks E, Reeves G, Pirie K, Beral V (2008) Family history and breast cancer tumour characteristics in screened women. Int J Cancer 123:2950–2954
Phipps AI, Li CI, Kerlikowske K, Malone KE, Barlow WE, Buist DSM (2010) Risk factors for ductal, lobular, and mixed ductal-lobular breast cancer in a screening population. Cancer Epidemiol Biomarkers Prev 19:1643–1654
van der Groep P, Bouter A, van der Zanden R, Siccama I, Menko FH, Gille JJ, van Kalken C, van der Wall E, Verheijen RH, van Diest PJ (2006) Distinction between hereditary and sporadic breast cancer on the basis of clinicopathological data. J Clin Pathol 59:611–617
Shuen AY, Foulkes WD (2011) Inherited mutations in breast cancer genes—risk and response. J Mammary Gland Biol Neoplasia 16:3–15
Allen-Brady K, Camp NJ, Ward JH, Cannon-Albright LA (2005) Lobular breast cancer: excess familiality observed in the Utah Population Database. Int J Cancer 117:655–661
Cleton-Jansen AM (2002) E-cadherin and loss of heterozygosity at chromosome 16 in breast carcinogenesis: different genetic pathways in ductal and lobular breast cancer? Breast Cancer Res 4:5–8
Hemminki K, Sundquist J, Ji J (2007) Familial risk for gastric carcinoma: an updated study from Sweden. Br J Cancer 96:1272–1277
Han MA, Oh MG, Choi IJ, Park SR, Ryu KW, Nam B-H, Cho S-J, Kim CG, Lee JH, Kim Y-W (2012) Association of family history with cancer recurrence and survival in patients with gastric cancer. J Clin Oncol 30:701–708
Polkowski W, van Sandick JW, Offerhaus GJ, ten Kate FJ, Mulder J, Obertop H, van Lanschot JJ (1999) Prognostic value of Laurén classification and c-erbB-2 oncogene overexpression in adenocarcinoma of the esophagus and gastroesophageal junction. Ann Surg Oncol 6:290–297
Graziano F, Humar B, Guilford P (2003) The role of the E-cadherin gene (CDH1) in diffuse gastric cancer susceptibility: from the laboratory to clinical practice. Ann Oncol 14:1705–1713
van der Post RS, Vogelaar IP, Carneiro F, Guilford P, Huntsman D, Hoogerbrugge N, Caldas C, Schreiber KE, Hardwick RH, Ausems MG, Bardram L, Benusiglio PR, Bisseling TM, Blair V, Bleiker E, Boussioutas A, Cats A, Coit D, DeGregorio L, Figueiredo J, Ford JM, Heijkoop E, Hermens R, Humar B, Kaurah P, Keller G, Lai J, Ligtenberg MJ, O’Donovan M, Oliveira C, Pinheiro H, Ragunath K, Rasenberg E, Richardson S, Roviello F, Schackert H, Seruca R, Taylor A, Ter Huurne A, Tischkowitz M, Joe ST, van Dijck B, van Grieken NC, van Hillegersberg R, van Sandick JW, Vehof R, van Krieken JH, Fitzgerald RC (2015) Hereditary diffuse gastric cancer: updated clinical guidelines with an emphasis on germline CDH1 mutation carriers. J Med Genet 52:361–374
Guilford P, Hopkins J, Harraway J, McLeod M, McLeod N, Harawira P, Taite H, Scoular R, Miller A, Reeve AE (1998) E-cadherin germline mutations in familial gastric cancer. Nature 392:402–405
Sarrio D, Moreno-Bueno G, Hardisson D, Sanchez-Estevez C, Guo M, Herman JG, Gamallo C, Esteller M, Palacios J (2003) Epigenetic and genetic alterations of APC and CDH1 genes in lobular breast cancer: relationships with abnormal E-cadherin and catenin expression and microsatellite instability. Int J Cancer 106:208–215
Kerber RA, Slattery ML (1997) Comparison of self-reported and database-linked family history of cancer data in a case-control study. Am J Epidemiol 146:244–248
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The authors have no commercial associations, financial disclosures, or other conflicts of interest to report with regard to this article. There are no sources of support for the work in the form of grants, equipment, drugs, or any combination of these.
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The authors declare that have no conflict of interest. There are no sources of support for the work in the form of grants, equipment, drugs, or any combination of these. This retrospective study was conducted with the authorization of our Institutional Review Board.
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Chikman, B., Davidson, T., Kais, H. et al. Is there an association between invasive lobular carcinoma of the breast and a family history of gastric cancer?. Familial Cancer 15, 41–47 (2016). https://doi.org/10.1007/s10689-015-9833-9
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DOI: https://doi.org/10.1007/s10689-015-9833-9