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Reduction in rate of node metastases with breast screening: consistency of association with tumor size

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Abstract

Population screening has brought about changes in both the incidence and mortality rates of patients with breast cancer. Large numbers of small screen-detected tumors have inspired discussions about overdiagnosis based on potential biological differences between screen-detected and symptomatic cancers. In the current systematic review, we analyzed the relation and the interaction of tumor size and nodal status in correlation with screening. Smaller tumors were more frequently screen detected (pT1 78.5 %) than symptomatic (pT1 61.7 %, p < 0.001), with a RR of 1.6 (95 % CI 1.4–1.8, n = 41,209). In the screened population, pT1 tumors were also more frequent (68.5 vs 49.9 %, n = 51,171, p < 0.001). Positive lymph nodes were less frequent in screen-detected tumors (26.8 vs 46.3 %, n = 43,705, p < 0.001) as well as in screened populations as a whole (24.1 vs 44.9 %, n = 49,581, p < 0.001). The relation between size and nodal status was not different between the screen-detected and the symptomatic tumors [pT2+N+ OR 2.42 (95 % CI 1.69–3.48) vs OR 2.91 (95 % CI 2.41–3.51)], suggesting that biological differences, if present, are small. In this systematic review, we confirmed both the association of screening with smaller tumor size at presentation and the consequent reduction in lymph node metastases.

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References

  1. Anderson TJ, Lamb J, Donnan P, Alexander FE, Huggins A, Muir BB, Kirkpatrick AE, Chetty U, Hepburn W, Smith A (1991) Comparative pathology of breast cancer in a randomised trial of screening. Br J Cancer 64:108–113

    Article  PubMed  CAS  Google Scholar 

  2. Anderson TJ, Waller M, Ellis IO, Bobrow L, Moss S (2004) Influence of annual mammography from age 40 on breast cancer pathology. Hum Pathol 35:1252–1259

    Article  PubMed  Google Scholar 

  3. Arisio R, Sapino A, Cassoni P, Accinelli G, Cuccorese MC, Mano MP, Bussolati G (2000) What modifies the relation between tumour size and lymph node metastases in T1 breast carcinomas? J Clin Pathol 53:846–850

    Article  PubMed  CAS  Google Scholar 

  4. Aubard Y, Genet D, Eyraud JL, Clavere P, Tubiana-Mathieu N, Philippe HJ (2002) Impact of screening on breast cancer detection. Retrospective comparative study of two periods 10 years apart. Eur J Gynaecol Oncol 23:37–41

    PubMed  CAS  Google Scholar 

  5. Barth A, Craig PH, Silverstein MJ (1997) Predictors of axillary lymph node metastases in patients with T1 breast carcinoma. Cancer 79:1918–1922

    Article  PubMed  CAS  Google Scholar 

  6. BSFTG (2002) The frequency of breast cancer screening: results from the UKCCCR randomised trial. United Kingdom Co-ordinating Committee on Cancer Research. Eur J Cancer 38:1458–1464

    Article  Google Scholar 

  7. Bucchi L, Puliti D, Ravaioli A, Cortesi L, De LV, Falcini F, Ferretti S, Frigerio A, Mangone L, Petrella M, Petrucci C, de Sassoli BP, Traina A, Tumino R, Zanetti R, Zorzi M, Paci E (2008) Breast screening: axillary lymph node status of interval cancers by interval year. Breast 17:477–483

    Article  PubMed  Google Scholar 

  8. Cody HS III (1995) The impact of mammography in 1096 consecutive patients with breast cancer, 1979–1993: equal value for patients younger and older than age 50 years. Cancer 76:1579–1584

    Article  PubMed  Google Scholar 

  9. Collett K, Stefansson IM, Eide J, Braaten A, Wang H, Eide GE, Thoresen SO, Foulkes WD, Akslen LA (2005) A basal epithelial phenotype is more frequent in interval breast cancers compared with screen detected tumors. Cancer Epidemiol Biomarkers Prev 14:1108–1112

    Article  PubMed  CAS  Google Scholar 

  10. Cortesi L, Chiuri VE, Ruscelli S, Bellelli V, Negri R, Rashid I, Cirilli C, Fracca A, Gallo E, Federico M (2006) Prognosis of screen-detected breast cancers: results of a population based study. BMC Cancer 6:17

    Article  PubMed  Google Scholar 

  11. Dawson SJ, Duffy SW, Blows FM, Driver KE, Provenzano E, LeQuesne J, Greenberg DC, Pharoah P, Caldas C, Wishart GC (2009) Molecular characteristics of screen-detected vs symptomatic breast cancers and their impact on survival. Br J Cancer 101:1338–1344

    Article  PubMed  CAS  Google Scholar 

  12. Domingo L, Sala M, Servitja S, Corominas JM, Ferrer F, Martinez J, Macia F, Quintana MJ, Albanell J, Castells X (2010) Phenotypic characterization and risk factors for interval breast cancers in a population-based breast cancer screening program in Barcelona, Spain. Cancer Causes Control 21:1155–1164

    Article  PubMed  Google Scholar 

  13. Ernst MF, Roukema JA, Coebergh JW, Repelaer van Driel OJ, van Beek MW, van der Sangen MJ, Voogd AC (2002) Breast cancers found by screening: earlier detection, lower malignant potential or both? Breast Cancer Res Treat 76:19–25

    Article  PubMed  CAS  Google Scholar 

  14. Ernst MF, Voogd AC, Coebergh JW, Roukema JA (2004) Breast carcinoma diagnosis, treatment, and prognosis before and after the introduction of mass mammographic screening. Cancer 100:1337–1344

    Article  PubMed  Google Scholar 

  15. Freedman GM, Anderson PR, Goldstein LJ, Hanlon AL, Cianfrocca ME, Millenson MM, von MM, Torosian MH, Boraas MC, Nicolaou N, Patchefsky AS, Evers K (2003) Routine mammography is associated with earlier stage disease and greater eligibility for breast conservation in breast carcinoma patients age 40 years and older. Cancer 98:918–925

    Article  PubMed  Google Scholar 

  16. Gabriel H, Wilson TE, Helvie MA (1997) Breast cancer in women 65–74 years old: earlier detection by mammographic screening. AJR Am J Roentgenol 168:23–27

    PubMed  CAS  Google Scholar 

  17. Hakama M, Holli K, Isola J, Kallioniemi OP, Karkkainen A, Visakorpi T, Pukkala E, Saarenmaa I, Geiger U, Ikkala J (1995) Aggressiveness of screen-detected breast cancers. Lancet 345:221–224

    Article  PubMed  CAS  Google Scholar 

  18. Hanrahan EO, Gonzalez-Angulo AM, Giordano SH, Rouzier R, Broglio KR, Hortobagyi GN, Valero V (2007) Overall survival and cause-specific mortality of patients with stage T1a, bN0M0 breast carcinoma. J Clin Oncol 25:4952–4960

    Article  PubMed  Google Scholar 

  19. Hanrahan EO, Valero V, Gonzalez-Angulo AM, Hortobagyi GN (2006) Prognosis and management of patients with node-negative invasive breast carcinoma that is 1 cm or smaller in size (stage 1; T1a, bN0M0): a review of the literature. J Clin Oncol 24:2113–2122

    Article  PubMed  Google Scholar 

  20. Heimann R, Munsell M, McBride R (2002) Mammographically detected breast cancers and the risk of axillary lymph node involvement: is it just the tumor size? Cancer J 8:276–281

    Article  PubMed  Google Scholar 

  21. Hislop TG, Worth AJ, Kan L, Rousseau E (1997) Post screen-detected breast cancer within the Screening Mammography Program of British Columbia. Breast Cancer Res Treat 42:235–242

    Article  PubMed  CAS  Google Scholar 

  22. Jensena AR, Ewertz M, Cold S, Storm HH, Overgaard J (2003) Time trends and regional differences in registration, stage distribution, surgical management and survival of breast cancer in Denmark. Eur J Cancer 39:1783–1793

    Article  PubMed  CAS  Google Scholar 

  23. Klemi PJ, Parvinen I, Pylkkanen L, Kauhava L, Immonen-Raiha P, Rasanen O, Helenius H (2003) Significant improvement in breast cancer survival through population-based mammography screening. Breast 12:308–313

    Article  PubMed  Google Scholar 

  24. Klemi PJ, Toikkanen S, Rasanen O, Parvinen I, Joensuu H (1997) Mammography screening interval and the frequency of interval cancers in a population-based screening. Br J Cancer 75:762–766

    Article  PubMed  CAS  Google Scholar 

  25. Kricker A, Newman B, Gertig DM, Goumas C, Armes J, Armstrong BK (2008) Why do large breast cancers still present in a population offered screening? Int J Cancer 123:2907–2914

    Article  PubMed  CAS  Google Scholar 

  26. Lindgren A, Holmberg L, Thurfjell E (1997) The influence of mammography screening on the pathological panorama of breast cancer. APMIS 105:62–70

    Article  PubMed  CAS  Google Scholar 

  27. Maibenco D, Daoud Y, Phillips E, Saxe A (1999) Relationship between method of detection of breast cancer and stage of disease, method of treatment, and survival in women aged 40 to 49 years. Am Surg 65:1061–1066

    PubMed  CAS  Google Scholar 

  28. McCann J, Duffy S, Day N (2001) Predicted long-term mortality reduction associated with the second round of breast screening in East Anglia. Br J Cancer 84:423–428

    Article  PubMed  CAS  Google Scholar 

  29. Miller AB, Baines CJ, To T, Wall C (1992) Canadian National Breast Screening Study: 1. Breast cancer detection and death rates among women aged 40 to 49 years. CMAJ 147:1459–1476

    PubMed  CAS  Google Scholar 

  30. Miller AB, Baines CJ, To T, Wall C (1992) Canadian National Breast Screening Study: 2. Breast cancer detection and death rates among women aged 50 to 59 years. CMAJ 147:1477–1488

    PubMed  CAS  Google Scholar 

  31. Mook S, Van ‘tVeer L, Rutgers EJ, Ravdin PM, van de Vijver MJ, van Leeuwen FE, Visser O, Schmidt MK (2011) Independent prognostic value of screen detection in invasive breast cancer. J Natl Cancer Inst 103:585–597

    Article  PubMed  Google Scholar 

  32. Moss S, Waller M, Anderson TJ, Cuckle H (2005) Randomised controlled trial of mammographic screening in women from age 40: predicted mortality based on surrogate outcome measures. Br J Cancer 92:955–960

    Article  PubMed  CAS  Google Scholar 

  33. Nagtegaal ID, Allgood PC, Duffy SW, Kearins O, Sullivan EO, Tappenden N, Wallis M, Lawrence G (2011) Prognosis and pathology of screen-detected carcinomas: how different are they? Cancer 117:1360–1368

    Article  PubMed  Google Scholar 

  34. Ng EH, Ng FC, Tan PH, Low SC, Chiang G, Tan KP, Seow A, Emmanuel S, Tan CH, Ho GH, Ng LT, Wilde CC (1998) Results of intermediate measures from a population-based, randomized trial of mammographic screening prevalence and detection of breast carcinoma among Asian women: the Singapore Breast Screening Project. Cancer 82:1521–1528

    Article  PubMed  CAS  Google Scholar 

  35. Norden T, Thurfjell E, Hasselgren M, Lindgren A, Norgren A, Bergstrom R, Holmberg L (1997) Mammographic screening for breast cancer. What cancers do we find? Eur J Cancer 33:624–628

    Article  PubMed  CAS  Google Scholar 

  36. Olivotto IA, Mates D, Kan L, Fung J, Samant R, Burhenne LJ (1999) Prognosis, treatment, and recurrence of breast cancer for women attending or not attending the Screening Mammography Program of British Columbia. Breast Cancer Res Treat 54:73–81

    Article  PubMed  CAS  Google Scholar 

  37. Olsen AH, Agbaje OF, Myles JP, Lynge E, Duffy SW (2006) Overdiagnosis, sojourn time, and sensitivity in the Copenhagen mammography screening program. Breast J 12:338–342

    Article  PubMed  Google Scholar 

  38. Olsson A, Garne JP, Tengrup I, Zackrisson S, Manjer J (2009) Overweight in relation to tumour size and axillary lymph node involvement in postmenopausal breast cancer patients-differences between women invited to vs. not invited to mammography in a randomized screening trial. Cancer Epidemiol 33:9–15

    Article  PubMed  Google Scholar 

  39. Palka I, Kelemen G, Ormandi K, Lazar G, Nyari T, Thurzo L, Kahan Z (2008) Tumor characteristics in screen-detected and symptomatic breast cancers. Pathol Oncol Res 14:161–167

    Article  PubMed  Google Scholar 

  40. Porter PL, El-Bastawissi AY, Mandelson MT, Lin MG, Khalid N, Watney EA, Cousens L, White D, Taplin S, White E (1999) Breast tumor characteristics as predictors of mammographic detection: comparison of interval- and screen-detected cancers. J Natl Cancer Inst 91:2020–2028

    Article  PubMed  CAS  Google Scholar 

  41. RCRC (1997) Breast carcinoma stage in relation to time interval since last mammography: a registry-based study. Cancer 80:1432–1437

    Article  Google Scholar 

  42. Shen Y, Yang Y, Inoue LY, Munsell MF, Miller AB, Berry DA (2005) Role of detection method in predicting breast cancer survival: analysis of randomized screening trials. J Natl Cancer Inst 97:1195–1203

    Article  PubMed  Google Scholar 

  43. Silverstein MJ, Gierson ED, Waisman JR, Colburn WJ, Gamagami P (1995) Predicting axillary node positivity in patients with invasive carcinoma of the breast by using a combination of T category and palpability. J Am Coll Surg 180:700–704

    PubMed  CAS  Google Scholar 

  44. Smith RA, Duffy SW, Gabe R, Tabar L, Yen AMF, Chen HHT (2004) The randomized trials of breast cancer screening: what have we learned? Radiol Clin N Am 42:793–806

    Article  PubMed  Google Scholar 

  45. SOSSEG (2006) Reduction in breast cancer mortality from organized service screening with mammography: 1. Further confirmation with extended data. Cancer Epidemiol Biomarkers Prev 15:45–51

    Article  Google Scholar 

  46. SOSSEG (2006) Reduction in breast cancer mortality from the organised service screening with mammography: 2. Validation with alternative analytic methods. Cancer Epidemiol Biomarkers Prev 15:52–56

    Article  Google Scholar 

  47. Spillane AJ, Kennedy CW, Gillett DJ, Carmalt HL, Janu NC, Rickard MT, Donnellan MJ (2001) Screen-detected breast cancer compared to symptomatic presentation: an analysis of surgical treatment and end-points of effective mammographic screening. ANZ J Surg 71:398–402

    Article  PubMed  CAS  Google Scholar 

  48. Sweeney KJ, Kell MR, Aziz NA, Prunty N, Holloway P, Kennedy M, Flanagan F, Kerin MJ (2007) The clinical and pathological differences in prevalent round screen-detected and symptomatic invasive breast cancer. Ir Med J 100:550–552

    PubMed  CAS  Google Scholar 

  49. Tabar L, Duffy SW, Krusemo UB (1987) Detection method, tumour size and node metastases in breast cancers diagnosed during a trial of breast cancer screening. Eur J Cancer Clin Oncol 23:959–962

    Article  PubMed  CAS  Google Scholar 

  50. Thomson CS, Brewster DH, Dewar JA, Twelves CJ (2004) Improvements in survival for women with breast cancer in Scotland between 1987 and 1993: impact of earlier diagnosis and changes in treatment. Eur J Cancer 40:743–753

    Article  PubMed  CAS  Google Scholar 

  51. Vacek PM, Geller BM, Weaver DL, Foster RS Jr (2002) Increased mammography use and its impact on earlier breast cancer detection in Vermont, 1975–1999. Cancer 94:2160–2168

    Article  PubMed  Google Scholar 

  52. van Dijck J, Verbeek A, Hendriks J, Holland R, Mravunac M (1996) Mammographic screening after the age of 65 years: early outcomes in the Nijmegen programme. Br J Cancer 74:1838–1842

    Article  PubMed  Google Scholar 

  53. Weaver DL, Rosenberg RD, Barlow WE, Ichikawa L, Carney PA, Kerlikowske K, Buist DS, Geller BM, Key CR, Maygarden SJ, Ballard-Barbash R (2006) Pathologic findings from the Breast Cancer Surveillance Consortium: population-based outcomes in women undergoing biopsy after screening mammography. Cancer 106:732–742

    Article  PubMed  Google Scholar 

  54. Weigel S, Batzler WU, Decker T, Hense HW, Heindel W (2009) First epidemiological analysis of breast cancer incidence and tumor characteristics after implementation of population-based digital mammography screening. Rofo 181:1144–1150

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

This study was supported by Cancer Research UK. Dr Nagtegaal was supported by a fellowship from the Dutch Cancer Society.

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Authors and Affiliations

  1. Department of Pathology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands

    I. D. Nagtegaal

  2. Centre for Cancer Prevention, Wolfson Institute of Preventive Medicine, Charterhouse Square, London, EC1M 6BQ, UK

    S. W. Duffy

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Correspondence to S. W. Duffy.

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Nagtegaal, I.D., Duffy, S.W. Reduction in rate of node metastases with breast screening: consistency of association with tumor size. Breast Cancer Res Treat 137, 653–663 (2013). https://doi.org/10.1007/s10549-012-2384-y

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