Which type of cancer is detected in breast screening programs? Review of the literature with focus on the most frequent histological features| Pathologica - Journal of the Italian Society of Anatomic Pathology and Diagnostic Cytopathology
Vol. 113: Issue 2 - April 2021
DOI: 10.32074/1591-951X-123
Review
Published: 2021-05-13
download
PDF

Which type of cancer is detected in breast screening programs? Review of the literature with focus on the most frequent histological features

Unit of Anatomic Pathology, Department of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, Italy
Unit of Anatomic Pathology, Department of Oncology, Bellaria Hospital, Bologna Italy
Unit of Anatomic Pathology, Department of Oncology, Bellaria Hospital, Bologna Italy
Unit of Breast Surgery, Department of Oncology, Bellaria Hospital, Bologna Italy
Unit of Senology, Department of Oncology, Bellaria Hospital, Bologna Italy
Radiation Oncology Unit, Bellaria Hospital, Bologna, Italy
Department of Medical Oncology, Azienda USL, Bologna, Italy; IRCCS Institute of Neurological Sciences, Bologna, Italy
Department of Medical Oncology, Azienda USL, Bologna, Italy; IRCCS Institute of Neurological Sciences, Bologna, Italy
Unit of Anatomic Pathology, Department of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, Italy
breast cancer in situ carcinoma invasive carcinoma interval cancer screening program

Abstract

Breast cancer is the most frequent type of cancer affecting female patients. The introduction of breast cancer screening programs led to a substantial reduction of mortality from breast cancer. Nevertheless, doubts are being raised on the real efficacy of breast screening programs. The aim of the present paper is to review the main pathological type of cancers detected in breast cancer screening programs. Specifically, attention will be given to: in situ carcinoma, invasive carcinoma histotypes and interval cancer.

Introduction

Breast cancer is the most frequent cancer affecting female patients, accounting for 23% of all cancers in women 1. Since its beginning, the mammography based screening program for breast cancer (breast screening program, BSP) has been considered an effective tool to reduce mortality in female patients. Nevertheless, during the last years some authors questioned the real effectiveness of screening in preventing death from breast cancer 2. Consideration on BSP efficacy is mainly based on epidemiological data, most of which do not consider the tumor histotype.

Pathologists know very well the great variety of breast cancer histotypes and their impact on prognosis 3.

Therefore, the aim of the present paper is to review the literature focusing on the different types of breast cancer detected in BSP.

Three different breast cancers will be considered: in situ carcinoma; invasive breast carcinoma (IBC); interval cancer (IC).

IN SITU CARCINOMA

Ductal carcinoma in situ (DCIS) represented < 5% of breast cancer in pre-screening era, while its incidence increased after BSP introduction, raising to 20% of breast cancers 4.

DCIS is a proliferation of neoplastic cells, confined within the ductal and lobular system 3. It is a non-obligate precursor of invasive breast carcinoma.

Indeed, DCIS can be detected as occasional finding in autopsies 5 or in reduction mammoplasties 6, thus leading the authors to consider a diagnosis of DCIS as an overdiagnosis of cancer 7,8.

On the other side, DCIS comprises a great variety of morphological patterns that can be subdivided into different grades 3 (Figs. 1, 2). DCIS grading is an important prognostic feature 4,9.

DCIS grading is related to the risk to develop IBC. Maxwell et al. 9 reviewed a series of untreated DCIS and demonstrated a correlation between DCIS grade and the development of IBC. IBC developed in 48% of patients with DCIS grade 3, in 32% of DCIS grade 2 and 18% of DCIS grade 1. Furthermore, DCIS grade was related to IBC grade, as most DCIS grade 2 and 3 give rise to high grade IBC 9.

This statement holds true despite the fact that DCIS grading is not uniformly used all over the world 10, but most high-grade cases are reproducibly classified 11. Van Maaren et al. 11 analyzed a cohort of 12,256 patients with DCIS. The incidence of breast cancer related deaths was very low (1.5% among all the cases), but it increased with increasing grade. Specifically, breast cancer related deaths were 0.7% in DCIS grade 1, 1.3% in DCIS grade 2 and 1.6% in DCIS grade 3.

Therefore, it is important to evaluate which types of DCIS are detected in BSP.

Von Luijt et al. 12 analyzed a cohort of 4232 women with screen detected DCIS: most DCIS were intermediate (32%) and high grade (52%). Similar data were obtained by Weigel et al. 13 confirming the importance of screening in detecting high grade DCIS. Furthermore, Weigel et al. 13 demonstrated that the incidence of high-grade DCIS remained high even in the second and subsequent screening rounds.

Age at the time of diagnosis is another important point to be considered.

According to von Lujit et al. 12, the risk of high-grade DCIS overdiagnosis is lower in younger women, aged 50-70 years, while it increases after the age of 70. Van Ravesteyn et al. 14 applying different statistical models, demonstrated a lower risk of DCIS overdiagnosis in women aged less than 74 years.

On the basis of the published data, most screen detected DCIS are high grade lesions, affecting women aged 50-70 years. Nevertheless, the problem of overdiagnosis for low grade DCS cases still exists.

Screen detected low grade DCIS poses several problems, as correct diagnosis and grading.

Correct diagnosis and differentiation with intraductal proliferative lesions can be a difficult challenge in daily practice. In spite of detailed descriptions published from a long time 15 and recently reviewed 16,17, differential diagnosis between epitheliosis (usual duct hyperplasia) and low grade DCIS, can still be a difficult task on pre-operative core biopsies. Accurate histological analysis, searching for the typical intraductal glandular structures, lined by polarized epithelial cells is fundamental for the diagnosis of low-grade DCIS. In doubtful cases, high molecular weight cytokeratins (as cytokeratin 14 or 5/6) negativity associated with strong estrogen receptor (ER) positivity in the neoplastic cells, can help to reach the correct diagnosis (Fig. 3).

DCIS grading can be difficult and still presents a high degree of variation among the different laboratories 10,18,19. Grading variability depends on many factors, the most important being the lack of uniform criteria. Several grading systems have been proposed for DCIS, none of which is universally accepted 10,18.

On the other hand, DCIS grading is of outmost prognostic value as it can help to choose the correct treatment (surgery vs active surveillance). In the Sagara et al. 20 series, 1169 DCIS cases were managed without surgery, while 56,053 cases received surgical excision. After a median follow-up of 72 months, in the low-grade DCIS group breast cancer-specific survival was almost similar for both non-surgery and surgery cases (98.8% without surgery compared to 98.6% with surgery P = 0.95), thus demonstrating that a minor proportion of low-grade DCIS progress to invasion.

When low-grade DCIS is diagnosed on pre-operative core biopsies, only a minority of cases are upstaged to IBC on surgical samples. Upstaging rates vary from 0% 21 to 21% 22. All IBC detected are well or moderately differentiated.

Evaluating data presently available in the literature, care should be taken as most of the studies consider relatively short follow-up intervals. Data retrieved from the Great Britain Breast Screening Programme 24 evidenced that women with screen detected DCIS present a long-term risks of invasive breast cancer higher than women in the general population. It is noteworthy to underline that the risk period spans for at least two decades after DCIS diagnosis and also comprises low and intermediate grade DCIS.

Data presently published indicate that, to exactly evaluate low-grade DCIS prognosis, further parameters should be added 25, such as correlation with clinical and mammographic findings 26 and molecular profile 27.

Lobular carcinoma in situ (LCIS) can be detected in BSP, even if less frequently than DCIS. Similarly to DCIS, LCIS covers a wide spectrum of lesions 3 each one carrying different aggressive potential. LCIS classical type can be an incidental finding, detected in association with benign calcifications 28.

Recent papers focused attention on the florid (F) and pleomorphic (P) variants of LCIS 29,30 (Fig. 4). F and P LCIS present necrosis and calcification, and therefore can be detected in BSP. F and P LCIS were considered aggressive lesions, but, due to their rarity, data were scanty and mainly based on small series. A recent study, based on 117 F and P LCIS all diagnosed on pre-operative biopsies, demonstrated that more than 60% of the F and P LCIS at presentation, can hide foci of IBC or high-grade DCIS. In addition, most invasive carcinomas were of the lobular histotype, grade 2 or 3, and thus aggressive variants of breast cancer, which are potentially lethal 30.

The data presently published indicate that BSPs detect mainly high grade in situ carcinoma (both of ductal or lobular type) in younger women. These data suggest that participation to BSP can reduce the risk of IBC 31,32.

INVASIVE BREAST CARCINOMA (IBC)

Most of the published data indicate that the most frequent type of screen detected IBC is luminal A type 33,34 (Fig. 5), characterized by high estrogen (ER) and progesterone receptors (PR), lack of HER2 amplification and low Ki-67 labelling index. Falck et al. 34 found that 92% of screen detected IBC were ER positive, compared to 86% of symptomatic cancers. Similarly, Ki-67 labelling index was lower than 20% in 75% of screen detected IBC, compared to 62% of symptomatic cases. On the contrary, HER2 amplification was more frequent in symptomatic cases than in screen detected IBC (24 vs 14%) 34.

Luminal A type of IBC is commonly considered a low-grade cancer, associated with good response to hormonal therapy and favourable prognosis. This statement is generally correct, but it should be remembered that luminal A type IBC comprises a wide spectrum of cancers. Invasive lobular carcinoma (ILC) usually meets the definition of luminal A cancer, showing high ER and PR expression, with Ki-67 lower than 20%. Nevertheless, ILC long term prognosis does not differ from that of IBC of no special type 35,36 depending mostly on TNM staging at presentation 35,37.

BSP can allow an early diagnosis. In Kobayashi et al.’s cases, 68.6% of screen detected IBC were staged I, compared with 38.2% only of symptomatic cases 38.

Therefore, as expected the IBC-related death rates are lower among screen detected cases, compared with symptomatic cases. Falck et al. 34 demonstrated that the mortality at 10 years was lower in patients with luminal carcinoma screen detected compared to symptomatic cases (3/92 VS 7/62). Moreover, worst prognosis was observed in non-luminal cases and node positive carcinomas 34.

Similar data were reported by several papers 38-43, all confirming the impact of BSP on breast cancer related mortality reduction.

INTERVAL CANCER (IC)

Interval cancer is defined as a cancer appearing between two screening examinations and after a negative mammography 44. IC can be subdivided into three different groups 44,45; missed cancers, radiographically occult cancers and true IC.

Missed cancers: cancers that were undetected due to technical or interpretations mistakes. This category cannot completely disappear, but can be significantly reduced with quality control programs and improved knowledge.

Radiographically occult cancers: cancers that are too small to be detected. This category comprises mainly ILC 44. ILC is characterized by infiltrative growth (Fig. 6), leading to little architectural distortion, therefore being difficult to detect on mammography 3. According to the data reported by Meshkat et al. 39 ILC constituted 21% of interval cancers, compared with 11% of screen detected cases. Similarly, Weber et al. 46 found lobular and ductulo-lobular carcinoma more frequent in IC.

Dense breast tissue can be an obstacle to accurate mammographic examination. On histology, dense breast is tissue characterized not only by increase in fibrous stroma, but also by lack of acinar involution and presence of cancer risk factors as atypical hyperplasia 47. Therefore, dense breast constitutes a fertile soil for radiographically occult cancers. Introduction of more accurate screening tools such as full-field digital mammography screening (FFDM) or tomosynthesis could improve early diagnosis 48-50.

Proper BSP tailored on the different breast densities are proposed 51.

True interval cancers: IC (interval cancers) appearing clearly on the diagnostic mammogram in absence of any suspect feature on the preceding screening examination 44,45. The morphological spectrum of true IC is wide and comprises almost all types of in situ and invasive breast cancer, the proportion of aggressive cases being higher.

DCIS presents as IC on rare occasions only 39. Symptomatic DCIS is usually larger, of higher grade and more frequently associated with invasive foci than the screen detected 39.

True ICs usually present a higher rate of grade 2 and 3, HER2 amplified, ER negative IBC 39. Furthermore, true ICs usually affect younger patients 46), show higher Ki-67 labelling index and present more frequently at stage II or higher 39,48-52.

Among true IC, triple negative breast cancers (TNBC) are encountered. TNBC constitute a heterogenous group of carcinomas that can be very difficult to be detected in BSP due to their specific pathological features, that can simulate benign lesions as fibroadenomas 53 (Fig. 7). According to a series published by Elfgen et al. 53, 8.6% of TNBC had a delay in diagnosis due to mammographic misclassification. Doebar et al. 54 demonstrated that the lowest frequency of a DCIS component was observed in the TNBC group (34.1%) thus suggesting that the TNBC rapidly develop the invasive component.

True IC have worst prognosis even among BRCA mutation carriers.

BRCA mutation carriers develop more frequently aggressive variants of IBC, showing a high percentage of TNBC 55. Therefore, BSP can have an important prognostic impact among BRCA mutation carriers. Pilewskie et al. 56 studied a population of 124 BC affecting BRCA mutation carries: 92 were detected in BSP, while 22 were spontaneous (11 of which were true IC), and 10 were occasional findings in prophylactic mastectomy. Even in the BRCA mutated population, IC affected younger women, tumours were larger and more frequently node positive than the screen detected ones 56. These data led to the conclusion that BSP can be useful also in BRCA mutated population.

Conclusion

Data recently published confirm the BSPs efficacy in early breast cancer detection, leading to a decrease in breast cancer related mortality 57,58. A study performed on the Italian population 59 demonstrated that organized BSPs led to a 30% reduction for stages II+ of IBC, thus leading to early diagnosis and easier cure potential.

On the other hand, higher rate of DCIS detection can cause overdiagnosis and overtreatment of harmless lesions. Improving knowledge on DCIS behavior can help in the selection of truly aggressive lesions deserving treatment 60.

Figures and tables

Figure 1.Low grade DCIS arising in sclerosing adenosis. (A): low power view showing closely packed glands. (B): cytokeratin 14 evidences the presence of a myoepithelial layer. (C): at higher power ducts are filled with monotonous neoplastic cells forming glandular lumina, psammomatous microcalcifications are present (arrow).

Figure 2.High grade DCIS arising in sclerosing adenosis. (A): low power view, the lesion presents a multinodular growth. (B): same lesion, stained with Cytokeratin 14 that evidences the myoepithelial layer. (C): at higher power ducts are lined by markedly atypical neoplastic cells, necrosis is present (arrow). D: cytokeratin 14 is helpful to avoid overdiagnosis of invasive carcinoma.

Figure 3.Low grade DCIS and differential diagnosis with florid epitheliosis. (A): low grade DCIS is characterized by a monotonous proliferation of neoplastic cells with bland nuclei. Neoplastic cells are polarized, with the secretroy pole oriented toward the lumen of the glandular strucure (arrow). (B): CK 14 stains the myoepithelial cells located at the periphery of the ducts, while the neoplastic cells are negative. (C): epitheliosis/usual duct hiperplasia is characterized by intraductal proliferation of cells devoid of atypia. Irregular spaces without any polarization are present. (D): in epithelosis CK 14 stains most of the intraductal cells.

Figure 4.Lobular carcinoma in situ, florid type. (A): the acinar units are filled with a solid proliferation of neoplastic cells, with uniform nuclei, necrosis is present (arrow). (B): E-Cadherin is negative in the neoplastic cells. (C): P-LCIS is characterized by enlarged terminal ductular-lobular units, filled with neoplastic cells, resembling high grade DCIS. (D): at higher power neoplastic cells are irregular. Binucleated neoplastic cells are easily detected (arrow). (E): E-Cadherin is negative, confirming the diagnosis of P-LCIS. (F): low molecular weight cytokeratins evidence small foci of invasion.

Figure 5.Tubular carcinoma (TC). (A): at low power view TC presents finely irregular margins. (B): at higher power, it is composed of angulated glands, lined by monotonous neoplastic cells. (C): almost all the neoplastic cells are strongly positive for estrogen receptor.

Figure 6.Invasive lobular carcinoma (ILC). (A): mammographically detected ILC associated with obliterative mastopathy. Obliterating ducts (arrow) show in situ lobular carcinoma of classical type; the surrounding tissue is infiltrated by neoplastic cells with minimal architectural distortion. (B): at higher power, neoplastic cells surround obliterating duct with in situ lobular carcinoma. (C): both in situ and invasive components are E-Cadherin negative. (D): both in situ and invasive components are strongly positive for estrogen receptor.

Figure 7.Metaplastic carcinoma. (A): at low power MC shows lobulated margins that can simulate a fibroadenoma. (B): at higher power MC is composed of markedly atypical cells, high nuclear grade in situ duct carcinoma is also present.

References

  1. Ferlay J, Shin HR, Bray F. Estimates of worldwide burden of cancer in 2008: GLO-BOCAN 2008. Int J Cancer. 2010; 127:2893-917. DOI | PubMed
  2. Bleyer A, Welch HG. Effect of three decades of screening mammography on breast-cancer in-cidence. N Engl J Med. 2012; 367:1998-2005. DOI | PubMed
  3. Allison K, Brogi E, Ellis IO. WHO Classification of Breast Tumours. IARC Press: Lyon; 2019.
  4. Park TS, Hwang ES. Current trends in the management of ductal carcinoma in situ. Oncol-ogy (Williston Park). 2016; 30:823-31. PubMed
  5. Sidiropoulou Z, Vasconcelos AP, Couceiro C. Prevalence of silent breast cancer in autopsy specimens, as studied by the disease being held by image-guided biopsies: the pilot study and literature review. Mol Clin Oncol. 2017; 7:193-199. DOI | PubMed |
  6. Sorin T, Fyad JP, Pujo J. Incidence of occult contralateral carcinomas of the breast following mastoplasty aimed at symmetrization. Ann Chir Plast Esthet. 2014; 59:e21-28. DOI | PubMed
  7. Hollingsworth A. Overestimating overdiagnosis in breast cancer screening. Cureus. 2017; 9:e966. DOI | PubMed |
  8. Groen EJ, Elshof LE, Visser LL. Finding the balance between over- and under-treatment of ductal carcinoma in situ (DCIS). Breast. 2017; 31:274-283. DOI | PubMed
  9. Maxwell AJ, Clements K, Hilton B, Sloane Project Steering Group. Risk factors for the development of invasive cancer in unresected ductal carcinoma in situ. Eur J Surg Oncol. 2018; 44:429-35. DOI | PubMed
  10. Cserni G, Sejben A. Grading Ductal Carcinoma In Situ (DCIS) of the Breast - What’s wrong with It?. Pathol Oncol Res. 2020; 26:665-671. DOI
  11. van Maaren MC, Lagendijk M, Tilanus-Linthorst MMA. Breast cancer-related deaths ac-cording to grade in ductal carcinoma in situ: a Dutch population-based study on patients diagnosed between 1999 and 2012. Eur J Cancer. 2018; 101:134-142. DOI | PubMed
  12. van Luijt PA, Heijnsdijk EA, Fracheboud J. The distribution of ductal carcinoma in situ (DCIS) grade in 4232 women and its impact on overdiagnosis in breast cancer screening. Breast Can-cer Res. 2016; 18:47. DOI | PubMed |
  13. Weigel S, Khil L, Hense HW. Detection rates of ductal carcinoma in situ with biennial digital mammography screening: radiologic findings support pathologic model of tumor progression. Radiology. 2018; 286:424-432. DOI | PubMed
  14. van Ravesteyn NT, Stout NK, Schechter CB. Benefits and harms of mammography screening after age 74 years: model estimates of overdiagnosis. J Natl Cancer Inst. 2015; 107:pii: djv103. DOI | PubMed |
  15. Azzopardi JG, Ahmed A, Millis RR. Problems in breast pathology. Major Probl Pathol. 1979; 11:i-xvi. PubMed
  16. Ellis IO. Intraductal proliferative lesions of the breast: morphology, associated risk and mole-cular biology. Mod Pathol. 2010; 23:S1-7. DOI | PubMed
  17. Rosa M, Agosto-Arroyo E. Ann Diagn Pathol.. 2019; 43:151407. DOI | PubMed
  18. van Dooijeweert C, van Diest PJ, Baas IO. Grading variation in 2,934 patients with ductal carcinoma in situ of the breast: the effect of laboratory- and pathologist-specific feedback reports. Diagn Pathol. 2020; 15:52. DOI | PubMed
  19. Alghamdi SA, Krishnamurthy K, Garces Narvaez SA. Low grade ductal carcinoma in situ. Am J Clin Pathol. 2020; 153:360-367. DOI | PubMed
  20. Sagara Y, Mallory MA, Wong S. Survival benefit of breast surgery for low-grade ductal carcinoma in situ: a population-based cohort study. JAMA Surg. 2015; 150:739-745. DOI | PubMed
  21. Soumian S, Verghese ET, Booth M. Concordance between vacuum assisted biopsy and postoperative histology: implications for the proposed Low Risk DCIS Trial (LORIS). Eur J Surg Oncol. 2013; 39:1337-1340. PubMed
  22. Brennan ME, Turner RM, Ciatto S. Ductal carcinoma in situ at core-needle biopsy: metaanalysis of underestimation and predictors of invasive breast cancer. Radiology. 2011; 260:119-128. PubMed
  23. Grimm LJ, Ghate SV, Hwang ES. Imaging features of patients undergoing active surveillance for ductal carcinoma in situ. Acad Radiol. 2017; 24:1364-1371. DOI
  24. Mannu GS, Wang Z, Broggio J. Invasive breast cancer and breast cancer mortality after ductal carcinoma in situ in women attend-ing for breast screening in England, 1988-2014: population based observational cohort study. BMJ. 2020; 369:m1570. DOI | PubMed
  25. Takada K, Kashiwagi S, Asano Y. Factors predictive of invasive ductal carcinoma in cases preopera-tively diagnosed as ductal carcinoma in situ. BMC Cancer. 2020; 20:513. DOI | PubMed
  26. Salvatorelli L, Puzzo L, Vecchio GM. Ductal carcinoma in situ of the breast: an update with emphasis on radiological and morphological features as predic-tive prognostic factors. Cancers (Basel). 2020; 12:609. DOI | PubMed
  27. Pareja F, Brown DN, Lee JY. Whole-exome sequencing analysis of the progression from non-low-grade ductal carcinoma in situ to invasive ductal carcinoma. Clin Cancer Res. 2020; 26:3682-3693. DOI | PubMed
  28. Rageth CJ, O’Flynn EAM, Pinker K. Second International Consensus Conference on lesions of uncertain malignant potential in the breast (B3 lesions). Breast Cancer Res Treat. 2019; 174:279-296. DOI | PubMed |
  29. Sapino A, Frigerio A, Peterse JL. Mammographically detected in situ lobular carcinomas of the breast. Virchows Arch. 2000; 436:421-30. PubMed
  30. Foschini MP, Miglio R, Fiore R. Pre-operative management of pleomorphic and florid lobular carcinoma in situ of the breast: report of a large multi-institutional series and review of the literature. Eur J Surg Oncol. 2019; 45:2279-2286. DOI | PubMed
  31. Duffy SW, Dibden A, Michalopoulos D. Screen detection of ductal carcinoma in situ and subsequent incidence of invasive interval breast cancers: a retrospective population-based study. Lancet Oncol. 2016; 17(1):109-14. DOI | PubMed |
  32. Weigel S, Heindel W, Heidrich J. Reduction of advanced breast cancer stages at subsequent participation in mammography screening. Rofo. 2016; 188:33-7. DOI | PubMed
  33. Johnson K, Zackrisson S, Rosso A. Tumor characteristics and molecular subtypes in breast cancer screening with digital breast tomosynthesis: the Malmö Breast Tomosynthesis Screening Trial. Radiology. 2019; 293:273-281. DOI | PubMed
  34. Falck AK, Röme A, Fernö M. St Gallen molecular subtypes in screening-detected and symptomatic breast cancer in a prospective cohort with long-term follow-up. Br J Surg. 2016; 103:513-23. DOI | PubMed |
  35. Wang K, Zhu GQ, Shi Y. Long-term survival differences between t1-2 invasive loblar breast cancer and corresponding ductal carcinoma after breast-conserving surgery: a propensity-scored matched longitudinal cohort study. Clin Breast Cancer. 2019; 19:e101-e115. DOI | PubMed
  36. Duraker N, Hot S, Akan A. A comparison of the clinicopathological features, metasta-sis sites and survival outcomes of invasive lobular, invasive ductal and mixed invasive ductal and lobular breast carcinoma. Eur J Breast Health. 2020; 16:22-31. DOI | PubMed |
  37. Carbognin L, Sperduti I, Arpino G. A propensity score analysis exploring the impact of adjuvant chemotherapy (aCT) in 739 patients (pts) affected by early stage pure Invasive Lobular breast Carcinoma (ILC). Ann Oncol. 2017; 28:vi27. DOI
  38. Kobayashi N, Hikichi M, Ushimado K. Differences in subtype distribution between screen-detected and symptomatic invasive breast cancer and their impact on survival. Clin Transl Oncol. 2017; 19:1232-1240. DOI | PubMed
  39. Meshkat B, Prichard RS, Al-Hilli Z. A comparison of clinical-pathological characteristics between symptomatic and interval breast cancer. Breast. 2015; 24:278-82. DOI | PubMed
  40. Doebar SC, van den Broek EC, Koppert LB. Extent of ductal carcinoma in situ according to breast cancer subtypes: a population-based cohort study. Breast Cancer Res Treat. 2016; 158:179-187. DOI | PubMed
  41. Inari H, Shimizu S, Suganuma N. A comparison of clinicopathological characteristics and long-term survival outcomes between symptomatic and screen-detected breast cancer in Japanese women. Breast Cancer. 2017; 24:98-103. DOI | PubMed
  42. Lau SS, Cheung PS, Wong TT. Comparison of clinical and pathological characteristics between screen-detected and self-detected breast cancers: a Hong Kong study. Hong Kong Med J. 2016; 22:202-9. DOI | PubMed
  43. Li J, Ugalde-Morales E, Wen WX. Differential burden of rare and common variants on tumor characteristics, survival, and mode of detection in breast cancer. Cancer Res. 2018; 78:6329-6338. DOI | PubMed
  44. Holland R, Mravunac M, Hendriks JH. So-called interval cancers of the breast. Pathlogic and radiologic analysis of sixty-four cases. Cancer. 1982; 49:2527-33. PubMed
  45. Peeters PH, Verbeek AL, Hendriks JH. The occurrence of interval cancers in the Nijmegen screening programme. Br J Cancer. 1989; 59:929-32. PubMed
  46. Weber RJ, van Bommel RM, Louwman MW. Characteristics and prognosis of interval cancers after biennial screen-film or full-field digital screening mammography. Breast Cancer Res Treat. 2016; 158:471-83. DOI | PubMed
  47. Ghosh K, Vierkant RA, Frank RD. Association between mammographic breast density and histologic features of benign breast disease. Breast Cancer Res. 2017; 19:134. DOI | PubMed
  48. Choi WJ, Cha JH, Kim HH. Analysis of prior mammography with negative result in women with interval breast cancer. Breast Cancer. 2016; 23:583-9. DOI | PubMed
  49. Caumo F, Zorzi M, Brunelli S. Digital breast tomosynthesis with synthesized two-dimensional images versus full-field digital mammography for population screening: outcomes from the Verona Screening Program. Radiology. 2018; 287:37-46. DOI | PubMed
  50. van Bommel RMG, Weber R, Voogd AC. Interval breast cancer characteristics before, during and after the transition from screen-film to full-field digital screening mammography. BMC Cancer. 2017; 17:315. DOI | PubMed |
  51. Nickson C, Velentzis LS, Brennan P. Improving breast cancer screening in Australia: a public health perspective. Public Health Res Pract. 2019; 29:pii: 2921911. DOI | PubMed
  52. Bellio G, Marion R, Giudici F. Interval breast cancer versus screen-detected cancer: comparison of clinicopathologic characteristics in a single-center analysis. Clin Breast Cancer. 2017; 17:564-571. DOI | PubMed
  53. Elfgen C, Varga Z, Reeve K. The impact of distinct triple-negative breast cancer subtypes on misdiagnosis and diagnostic delay. Breast Cancer Res Treat. 2019; 177:67-75. DOI | PubMed
  54. Doebar SC, van den Broek EC, Koppert LB. Extent of ductal carcinoma in situ according to breast cancer subtypes: a population-based cohort study. Breast Cancer Res Treat. 2016; 158:179-187. DOI
  55. Armstrong N, Ryder S, Forbes C. A systematic review of the international prevalence of BRCA mutation in breast cancer. Clin Epidemiol. 2019; 11:543-561. DOI | PubMed |
  56. Pilewskie M, Zabor EC, Gilbert E. Differences between screen-detected and interval breast cancers among BRCA mutation carriers. Breast Cancer Res Treat. 2019; 175:141-148. DOI | PubMed
  57. Tabár L, Vitak B, Chen TH. Swedish two-county trial: impact of mammographic scree-ning on breast cancer mortality during 3 decades. Radiology. 2011; 260:658-63. DOI | PubMed
  58. Sebuødegård S, Botteri E, Hofvind S. Breast cancer mortality after implementation of orga-nized population-based breast cancer screening in Norway. J Natl Cancer Inst. 2020; 112:839-846. DOI | PubMed
  59. Puliti D, Bucchi L, Mancini S, IMPACT COHORT Working Group. Advanced breast cancer rates in the epoch of service screening: The 400,000 women cohort study from Italy. Eur J Cancer. 2017; 75:109-116. DOI | PubMed
  60. van Seijen M, Lips EH, Thompson AM, PRECISION team. Ductal carcinoma in situ: to treat or not to treat, that is the question. Br J Cancer. 2019; 121:285-292. DOI | PubMed |

Affiliations

$authorString->getOrcid() =>

$authorString->getFullName() => Angelo Gianluca Corradini

$authorString->getUrl() =>

Angelo Gianluca Corradini

Unit of Anatomic Pathology, Department of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, Italy
non esiste orcidID ""

$authorString->getOrcid() =>

$authorString->getFullName() => Anna Cremonini

$authorString->getUrl() =>

Anna Cremonini

Unit of Anatomic Pathology, Department of Oncology, Bellaria Hospital, Bologna Italy
non esiste orcidID ""

$authorString->getOrcid() =>

$authorString->getFullName() => Maria Grazia Cattani

$authorString->getUrl() =>

Maria Grazia Cattani

Unit of Anatomic Pathology, Department of Oncology, Bellaria Hospital, Bologna Italy
non esiste orcidID ""

$authorString->getOrcid() =>

$authorString->getFullName() => Maria Cristina Cucchi

$authorString->getUrl() =>

Maria Cristina Cucchi

Unit of Breast Surgery, Department of Oncology, Bellaria Hospital, Bologna Italy
non esiste orcidID ""

$authorString->getOrcid() =>

$authorString->getFullName() => Gianni Saguatti

$authorString->getUrl() =>

Gianni Saguatti

Unit of Senology, Department of Oncology, Bellaria Hospital, Bologna Italy
non esiste orcidID ""

$authorString->getOrcid() =>

$authorString->getFullName() => Antonella Baldissera

$authorString->getUrl() =>

Antonella Baldissera

Radiation Oncology Unit, Bellaria Hospital, Bologna, Italy
non esiste orcidID ""

$authorString->getOrcid() =>

$authorString->getFullName() => Antonella Mura

$authorString->getUrl() =>

Antonella Mura

Department of Medical Oncology, Azienda USL, Bologna, Italy; IRCCS Institute of Neurological Sciences, Bologna, Italy
non esiste orcidID ""

$authorString->getOrcid() =>

$authorString->getFullName() => Selena Ciabatti

$authorString->getUrl() =>

Selena Ciabatti

Department of Medical Oncology, Azienda USL, Bologna, Italy; IRCCS Institute of Neurological Sciences, Bologna, Italy
non esiste orcidID ""

$authorString->getOrcid() =>

$authorString->getFullName() => Maria Pia Foschini

$authorString->getUrl() =>

Maria Pia Foschini

Unit of Anatomic Pathology, Department of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, Italy
non esiste orcidID ""

License

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Copyright

© Società Italiana di Anatomia Patologica e Citopatologia Diagnostica, Divisione Italiana della International Academy of Pathology , 2021

How to Cite

[1]
Corradini, A.G., Cremonini, A., Cattani, M.G., Cucchi, M.C., Saguatti, G., Baldissera, A., Mura, A., Ciabatti, S. and Foschini, M.P. 2021. Which type of cancer is detected in breast screening programs? Review of the literature with focus on the most frequent histological features. Pathologica - Journal of the Italian Society of Anatomic Pathology and Diagnostic Cytopathology. 113, 2 (May 2021), 85-94. DOI:https://doi.org/10.32074/1591-951X-123.
  • Abstract viewed - 1338 times
  • PDF downloaded - 742 times