|Year : 2015 | Volume
| Issue : 2 | Page : 74-80
Screening mammography in Ibadan: Our experience
MO Obajimi1, AT Adeniji-Sofoluwe1, AO Oluwasola2, BO Adedokun3, OA Mosuro4, AO Adeoye2, NT Ntekim5, TO Soyemi6, OO Osofundiya6, OS Bassey6
1 University of Ibadan, College of Medicine; Department of Radiology, University College Hospital, Ibadan, Nigeria
2 University of Ibadan, College of Medicine; Department of Pathology, University College Hospital, Ibadan, Nigeria
3 University of Ibadan, College of Medicine; Department of Epidemiology Medical Statistics and Environmental Health, University College Hospital, Ibadan, Nigeria
4 Department of Family Medicine, University College Hospital, Ibadan, Nigeria
5 University of Ibadan, College of Medicine; Department of Radiation Oncology, University College Hospital, Ibadan, Nigeria
6 Department of Radiology, University College Hospital, Ibadan, Nigeria
|Date of Web Publication||10-Nov-2015|
A T Adeniji-Sofoluwe
University of Ibadan, College of Medicine, Department of Radiology, University College Hospital, Ibadan
Source of Support: None, Conflict of Interest: None
Background: Early detection is an essential step in decreasing the mortality and morbidity of breast cancer. Mammography is a proven effective tool for early breast cancer detection. It has high sensitivity and specificity and remains the gold standard for breast cancer screening. This study aims at describing the findings at screening mammography in women in Ibadan, South-West Nigeria. Materials and Methods: A prospective descriptive single centre study of 568 asymptomatic women who had screening mammography over a 5 year period (2006–2011) in the Department of Radiology, University College Hospital, Ibadan, Nigeria. Two views; the cranio-caudal and the medio-lateral oblique views were obtained. Mammographic findings were reported using the American College of Radiology Breast Imaging Reporting and Data System (BI-RADS) lexicon and assigned a final BI-RADS category according to overall findings. Data was analysed using Statistical Package for the Social Science SPSS Inc. Released 2008. SPSS Statistics for Windows, Version 17.0. Chicago USA: SPSS Inc. Results: A total of 568 women participated in the study with age range from 22 to 82 years (mean 47.8 years). About a third (35.6%) of the women were post-menopausal; and a positive family history of breast cancer was reported in 28 (6.2%) women. The most frequent mammographic breast pattern was BI-RADS I (fatty replaced) in 181 (36.5%) women. Two hundred and twenty women had final BI-RADS category of two (benign), with 49% being fibroadenomas. Over 70% of 164 women called back for diagnostic work up absconded for various socioeconomic and religious factors. Nine women with suspicious breast masses were detected and had treatment constituted immediately. Conclusion: Mammography is just gaining ground in Nigeria; future increased patronage by women is anticipated with intense advocacy and widespread breast cancer awareness.
Keywords: Asymptomatic, mammography, screening
|How to cite this article:|
Obajimi M O, Adeniji-Sofoluwe A T, Oluwasola A O, Adedokun B O, Mosuro O A, Adeoye A O, Ntekim N T, Soyemi T O, Osofundiya O O, Bassey O S. Screening mammography in Ibadan: Our experience. Niger J Basic Clin Sci 2015;12:74-80
|How to cite this URL:|
Obajimi M O, Adeniji-Sofoluwe A T, Oluwasola A O, Adedokun B O, Mosuro O A, Adeoye A O, Ntekim N T, Soyemi T O, Osofundiya O O, Bassey O S. Screening mammography in Ibadan: Our experience. Niger J Basic Clin Sci [serial online] 2015 [cited 2022 Aug 14];12:74-80. Available from: https://www.njbcs.net/text.asp?2015/12/2/74/169297
| Introduction|| |
Breast cancer is the most common cause of cancer-related deaths among women around the globe. It accounts for more than 1–6% of all female deaths worldwide., It is also becoming an increasingly urgent problem in low-resource countries like Nigeria; where reports confirm increasing the incidence of up to 5%/year., In the recent past, breast cancer screening in Nigeria mainly consisted of self-breast examination (SBE) and clinical breast examination. However, studies have shown the low sensitivity of these approaches with a detection rate of only 0.1% for breast cancer.,,,,
There is a dearth of literature on mammography screening findings in West African and Nigerian women in particular. This might be attributed to the recent availability of mammographic facilities in Nigeria. Most of the facilities that are functional are found in privately owned centres that are more service than research oriented; as such, data on the patients evaluated are not published. Despite these shortcomings, a few studies are present in the literature.
In 2010, Akinola et al., carried out a study on mammograms and breast arterial calcifications (BAC) in 54 consecutive women seen at the Lagos University Teaching Hospital in Ikeja-Lagos. The study resolved that only 20% of the mammograms had BAC, which were related to increasing age. Mammographic patterns in 498 women imaged at the University College Hospital in Ibadan were assessed by Obajimi et al., in 2010 and found higher density patterns in nulliparous and younger women. Parasitic calcifications detected on mammograms of 39 women were also described in Ibadan, South-West Nigeria. In 2013, 180 mammograms of Ghanaian women were retrospectively reviewed by Brakohiapa et al., and found screeners to be the majority with benign findings more frequently detected. Two review articles on the need for standardisation of breast ultrasound and mammography reports in Nigeria have also been published by Obajimi et al., and Akhigbe and Igbinedion in Ibadan and Benin respectively.,
On the other hand, a lot of papers on epidemiology and breast cancer, knowledge attitude and beliefs or practice studies about breast cancer, clinical and SBE and mammographic screening have also been published in Enugu, Ibadan, Abakaliki and Osogbo.,,,,
Magnetic resonance imaging (MRI) is a breast imaging modality that utilises non-ionising radiation, but is expensive and not readily available. However, it is more accurate than ultrasound and mammography for the measurement of actual tumour size and follow-up of residual disease in patients after neo-adjuvant chemotherapy. It has its role in the evaluation of patients at a high risk of developing breast cancer. It is the modality of choice for axillary lymph node evaluation, staging of breast cancer and metastases.,,
Evidence abound that mammography is an effective screening tool. Several randomised control trials have repeatedly demonstrated a substantial and significant reduction in breast cancer mortality with mammographic screening.,,,, A 20% reduction in breast cancer death rate has been reported in women over 40-year-old. It is against this background that this single centre study is designed and aimed at describing the findings at screening mammography in women in Ibadan, South-West Nigeria.
| Materials and Methods|| |
This is a prospective descriptive study over a 5 year period (2006–2011) in the Department of Radiology, University College Hospital, Ibadan, Nigeria where 568 asymptomatic women who had screening mammography were recruited. They completed a breast data form as well as a structured study questionnaire where data on sociodemographic characteristics, obstetric and gynaecologic history and other selected risk factors for breast cancer were extracted.
Screening mammography was done using the General Electric senographe DMR + mammographic unit with a film screen technique. Two screening views; the craniocaudal (CC) and the medio-lateral oblique (MLO) were obtained for each breast. Additional views such as the spot magnification and or the spot compression were also obtained when needed. Informed consent was obtained from the women before imaging commenced.
The breast density was categorised by the interpreting radiologists MO and ATS using the American College of Radiology (ACR) mammographic breast pattern American College of Radiology Breast Imaging Reporting and Data System (BI-RADS) categories; BI-RADS 1: Entirely fatty breast pattern (<25% fibroglandular tissue); BI-RADS 2: Scattered fibroglandular pattern (25–50% fibroglandular tissue); BI-RADS 3: Heterogeneous fibroglandular pattern (51–75% fibroglandular tissue) and BI-RADS 4: Extremely dense (>75% fibroglandular tissue) [Figure 1].
|Figure 1: Mammographic breast pattern breast imaging reporting and data system (BI-RADS) categories; (a) BI-RADS 1; (b) BI-RADS 2; (c) BI-RADS; (d) BI-RADS 4|
Click here to view
The mammographic findings were also reported using the mammographic ACR BI-RADS Lexicon. Each mammogram was then assigned a final BI-RADS category according to overall findings by the radiologists; BI-RADS 0: (Inconclusive), BI-RADS 1 (Negative), BI-RADS 2: (Benign finding), BI-RADS 3: (Probably benign), BI-RADS 4:(Suspicious finding), BI-RADS 5: (Highly suggestive of malignancy finding) and BI-RADS 6: (Proven cancer).
A workup sono-mammography was recommended for women with BI-RADS 0 and 3, ultrasound guided core biopsy was done in some women with BI-RADS 4 and 5 and specimens sent to Pathology Department for Histopathology and immuno-chemistry reports. The sono-mammographic findings were also correlated with those found at conventional Mammography.
Data were entered into the Statistical Package for the Social Science SPSS Inc. Released 2008. SPSS Statistics for Windows, Version 17.0. Chicago USA: SPSS Inc., edited and analysis carried out. Association between mammographic breast density pattern, final BI-RADS category and selected sociodemographic and clinical variables were tested using the Chi-square test.
| Results|| |
A total of 568 women who had screening mammography done were recruited into the study. Their age ranged from 22 to 82 years with a mean of 47.8 years SD ± 8.7.
[Figure 2] shows the age distribution of the women in the study. The 40–44 age group recorded the highest proportion of women (25.9%). Only 3.9% were aged <35 years.
Almost 2/3rd (64.4%) of the women were pre-menopausal while about a 1/3rd (35.6%) were post-menopausal. Of the total number of women who were post-menopausal, 4.9% had a history of hysterectomy. Majority of the women (95.8%) were parous.
A positive family history of breast cancer in first and second degree relatives was reported in only 28 (6.2%) women, with 19 (67.9%) of the women below 35 years in this study. They all had limited screening mammograms comprising of only MLO views.
Only 44 (7.7%) women had been on hormonal therapy while 84 (18.8%) reported a previous mammography.
[Table 1] shows the spectrum of mammographic findings and recommendations made in the study population. The most frequent breast pattern using the ACR BI-RADS category was BI-RADS I (fatty replaced) in 181 (36.5%) women, while BI-RADS I and II 348 (70.2%); the less dense breast patterns were reported in the majority of the women.
|Table 1: Spectrum of mammographic findings and recommendations in study population|
Click here to view
One hundred and thirty-seven (25.8%) women had negative mammograms with final BI-RADS category of 1. However, the mammograms of 220 (41.5%) women showed benign findings with final BI-RADS category of 2. Final BI-RADS 3 category (probably benign) was assigned to 74 (14%) women. Suspicious findings and highly suggestive finding for malignancy (BI-RADS 4 and 5 respectively) were reported in only 9 (1.7%) women.
One to two years follow-up mammography visits was recommended in 307 women (57.6%) while whole breast or targeted breast ultrasound was advised in 212 (39.8%) women. Additional mammographic views and ultrasound guided biopsy were recommended in 12 (2.3%) and 2 (0.4%) women respectively.
[Figure 3] is a representation of the parenchymal breast lesions found in women with BI-RADS category 2. Fibroadenoma was the most common benign lesion seen in both breasts more on the right (60.3%). The second most common benign breast parenchymal lesion was intramammary lymph nodes, which were found more commonly on the left side 10 (20%). Simple cysts seen in 10 women (17.2%) were also more frequent on the right side. The least common breast lesions were papillomas (1.6%) and skin thickening (2%) which were found only on the right and left respectively. The upper outer quadrant was the most common site for these breast lesions. Benign calcifications found in 43 (19.7%) women were mainly vascular (30.2%). In the axillae, benign lymphadenopathy were the majority (61%). The nodes were mostly reactive and were bilateral in 56.8% of the women. Among the women with reactive lymph nodes, parenchymal breast lesions were recorded in only 89 (39%).
|Figure 3: Percentages and side location of breast lesions in women with final BI-RADS category 2 on Mammography|
Click here to view
[Table 2] is a representation of women with BI-RADS 0 and 3 categories; back for a diagnostic work up. One hundred and sixty-four (31%) women in both categories were called back for a diagnostic workup. Only 33 (20.1%) returned for further work up while over 70% absconded and were lost to follow-up. The most frequent reason for call back in the women that returned for follow-up was increased and or asymmetric breast density recorded in 19 (57.6%). The rest of the women in the group 14 (42.2%) had breast lesions that needed further characterization.
|Table 2: Women with final BI-RADS categories 0 and 3: Called back for diagnostic work up|
Click here to view
In the same group, 19 women whose mammograms were initially categorized as BI-RADS 0 were finally assigned to BI-RADS 1 following sono-mammography due to the absence of any abnormality or final BI-RADS 2 when enlarged benign axillary nodes were found. Thirteen women (92.9%) of the cohort had only benign enlarged axillary lymph nodes and no mass lesion. The only woman with parenchymal mass in the above group with BI-RADS 0 and 3 was a benign axillary tail lipoma. Her final assessment was BI-RADS 2. Of the women with final BI-RADS of 4 and 5 (suspicious and highly suggestive of malignancy lesions), 5 (62.5%) had mass lesions in the right breast with associated micro-calcifications. Seventy-five percent of the micro-calcifications were in the upper outer and inner quadrants; while 37.5% of the suspicious micro-calcifications were in the lower quadrants of the left breast but with no mass lesions. Core biopsy was done in two women in the fifth and seventh decades; invasive ductal carcinoma and secretory breast cancer were confirmed in them respectively. A benign and malignant lesion seen at mammography are depicted in [Figure 4].
|Figure 4: Breast lesions on mammography: (a) Benign: Well-circumscribed round low density mass in the upper outer quadrant (UOQ) of the left breast in a 60-year-old woman-breast cyst (left crano-caudial view [LCC]); (b) and reactive axillary lymph nodes (left medio-lateral oblique [LMLO] view); (c) Breast lesions on mammography malignant: Spiculated high density mass in the lower inner quadrant (LIQ) of the left breast in a 40-year-old woman-invasive ductal carcinoma (LCC view); (d) (LMLO view)|
Click here to view
| Discussion|| |
This study was undertaken to describe the findings at screening mammography in women in Ibadan, South-West Nigeria; identifying those with features suspicious of breast cancer, and recommending immediate therapy. It is proven that mammography screening aids in the detection of cancers at an early stage resulting in the better chance of successful treatment and survival.
The reported benefits of mammography appear to be more pronounced among women aged 50 years and above but less effective in the younger age group due to increased breast density in the latter which is also noted in lactating breasts., In the United States, a statistically significant mortality reduction has been reported in women aged 40–49 years due to regular breast cancer screening in women of this age group. Screening mammography significantly reduces breast cancer mortality in women aged 50–74 years with the advantageous effects persisting after long-term follow-up., The Cochrane International workshop on screening for breast cancer also reported a reduction in breast cancer mortality by a third in women aged 50–69 years.
The sensitivity and specificity of mammography varies in symptomatic and asymptomatic women and ranges from 75% to 90% and 90% to 95%, respectively. Although mammography remains the gold standard for breast cancer screening, there are some conflicting reports about its efficacy in cancer screening. One study reported missed breast cancer lesions in about 25% (false negatives) of the population studied. Breast density, lesion features, lesion location and observer error accounted for the findings. Despite these controversies, the balance of the evidence still favours screening mammography.
Ages 45–49 years is the peak age incidence for the development of breast cancer from the standpoint of age distribution. Although black women have a lower overall incidence of breast cancer compared with Caucasian women, the incidence rate of early onset breast cancer is actually higher in black women, a decade earlier than Caucasians., It has been proven that there is an approximate 24% and up to 30% reduction in the mortality rate with the use of mammography screening in women in the fifth decade and those 50–69 years respectively., Other risk factors for breast cancer are positive family history of breast cancer and hormonal factors.,
A small percentage (3.9%) of the women were <35 years old. These women are those with positive family history of breast cancer hence their presentation for screening earlier than the prescribed 40 years. They presented for screening mammography based on an increased level of awareness of breast cancer. Guidelines recently released by the American Cancer Society have suggested initiating breast cancer screening at 30 years for women at increased risks though with ultrasonography or MRI due to the dense breast pattern.,
About 6.2% had a positive family history of breast cancer, which included both first and second degree relatives. This is low when compared with reports among Caucasians with a prevalence rate as high as 26.4%.
Ideally screening mammography should be performed on women 40 years and above, but there is a caveat, according the ACR on mammography screening. Women with a positive family history of breast cancer are supposed to begin screening 10 years earlier than their family member who have/had breast cancer.,
In our study, a small percentage the women 4.2% and 7.7% were nulliparous and on hormone replacement therapy respectively. These figures are low compared to Caucasian women. This perhaps explains in part why breast cancer has a lower incidence in developing countries where most women are parous. Post-menopausal women in this part of the world rarely seek for hormone replacement therapy, which is in sharp contrast to Caucasian women.
A high prevalence of BI-RADS 1 and 2 breast density pattern associated with a low risk of breast cancer was demonstrated in our cohort with only 29.8% with BI-RADS 3 and 4, the dense breast pattern. This is similar to the result obtained by Obajimi et al., where only 30.2% of women studied had a similar dense breast pattern. This reiterates previous report of the relatively lower incidence of breast cancer among African women.
It has been documented that over 70% of parenchymal breast lesions are benign. In our study however, only 39% of the women had benign parenchymal breast lesions. This lower prevalence may be due to the fact that the women recruited into the study were asymptomatic and probably as a result of the small sample size. Fibroadenoma has been described as the most common benign breast mass in pre-menopausal women with the upper outer quadrant of the breast as the most common site. In older patients, popcorn calcification maybe seen within a fibroadenoma. Our study showed similar findings as fibroadenoma was the most common benign lesion found in both breasts; 60.3% and 56% on the right and left sides respectively. At histology, invasive ductal carcinoma and secretory breast cancer were identified. The former is the usual finding in breast cancer but secretory carcinoma is an unusual but distinct subtype of breast carcinoma, with characteristic histomorphology and generally excellent prognosis. Both children and adults may be affected with age range of 3 to 83 years. The tumour distinctively has large amounts of intracellular and extracellular, eosinophilic secretion material that stains positive for periodic acid–Schiff. Most tumors stain positive for S100 and negative for estrogen receptor, progesterone receptor, and ERBB2 (formerlyHER2/neu- triple negative).
This study began at a time when we just started to perform mammographic studies in the department. At the onset, training in breast imaging was still on going and the reporting style was not yet standardised hence the large missing data for breast pattern categorisation and final BI-RADs assessment categories. As time went on the proficiency in reporting mammograms improved.
One of the major challenges in a developing country like ours is a loss of patients to follow-up. This is due to factors such as ignorance, socioeconomic and religious reasons. This makes it impossible to determine the actual prevalence of benign lesions in this study. In another study by Obajimi et al., in 2013, only 31.8% of women studied in the same setting had tertiary education. This may account for only 5.1% of the women with previous knowledge of mammography, however, 71.4% of them had tertiary education.
Anderson etal., attributed low entry of women for early detection and cancer treatment programmes to lack of finance and organisation inherent in health care system, coupled with low awareness of breast cancer due to unavailability of health care providers with whom women have contact.
| Conclusion|| |
This mammographic screening study detected nine women with suspicious breast cancer masses who had treatment constituted immediately. Though just gaining grounds in our setting, future increased patronage by women is anticipated. However, intense advocacy and widespread breast cancer awareness is a sine qua none to compliance and cooperation of the women at the initial and follow-up imaging visits.
| References|| |
American Cancer Society. Cancer Facts and Figures, 2009. Atlanta: American Cancer Society; 2009.
Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005;55:74-108.
Ihekwaba FN. Breast cancer in Nigerian women. Br J Surg 1992;79:771-5.
Adebamowo CA, Ajayi OO. Breast cancer in Nigeria. West Afr J Med 2000;19:179-91.
Tabar L, Yen MF, Vitak B, Chen HH, Smith RA, Duffy SW. Mammography service screening and mortality in breast cancer patients: 20-year follow-up before and after introduction of screening. Lancet 2003;361:1405-10.
Tabár L, Fagerberg CJ, Gad A, Baldetorp L, Holmberg LH, Gröntoft O, et al.
Reduction in mortality from breast cancer after mass screening with mammography. Randomised trial from the Breast Cancer Screening Working Group of the Swedish National Board of Health and Welfare. Lancet 1985;1:829-32.
Tabar L, Fagerberg G, Duffy SW, Day NE. The Swedish two county trial of mammographic screening for breast cancer: Recent results and calculation of benefit. J Epidemiol Community Health 1989;43:107-14.
Tabár L, Vitak B, Chen HH, Duffy SW, Yen MF, Chiang CF, et al.
The Swedish two-county trial twenty years later. Updated mortality results and new insights from long-term follow-up. Radiol Clin North Am 2000;38:625-51.
Tabar L, Fagerberg G, Chen HH, Duffy SW, Smart CR, Gad A, et al.
Efficacy of breast cancer screening by age. New results from the Swedish two-county trial. Cancer 1995;75:2507-17.
Akinola RA, Ogbera OA, Onakoya JA, Enabulele CE, Fadeyibi IO. Mammograms and breast arterial calcifications: Looking beyond breast cancer: A preliminary report. BMC Res Notes 2011;4:207.
Obajimi MO, Adeniji-Sofoluwe AT, Oluwasola AO, Adedokun BO, Soyemi TO, Olopade F, et al.
Mammographic breast pattern in Nigerian women in Ibadan, Nigeria. Breast Dis 2011;33:9-15.
Adeniji-Sofoluwe AT, Obajimi MO, Oluwasola AO, Soyemi TO. Mammographic parasitic calcifications in South West Nigeria: Prospective and descriptive study. Pan Afr Med J 2013;15:126.
Brakohiapa EK, Armah GE, Clegg-Lamptey JN, Brakohiapa WO. Pattern of breast diseases in Accra: Review of mammography reports. Ghana Med J 2013;47:101-6.
Obajimi MO, Akute OO, Afolabi AO, Adenipekun AA, Oluwasola AO, Akang EE, et al
. BIRADS Lexicon, an urgent call for the standardization of breast ultrasound in Nigeria. Ann Ib Postgrad Med 2005;3:82-8.
Akhigbe AO, Igbinedion BO. Mammographic screening and reporting: A need for standardisation. A review. Niger Postgrad Med J 2013;20:346-51.
Okobia MN, Bunker CH, Okonofua FE, Osime U. Knowledge, attitude and practice of Nigerian women towards breast cancer: A cross-sectional study. World J Surg Oncol 2006;4:11.
Obajimi MO, Ajayi IO, Oluwasola AO, Adedokun BO, Adeniji-Sofoluwe AT, Mosuro OA, et al.
Level of awareness of mammography among women attending outpatient clinics in a teaching hospital in Ibadan, South-West Nigeria. BMC Public Health 2013;13:40.
Obaji N, Elom H, Agwu U, Nwigwe C, Ezeonu P, Umeora O. Awareness and practice of breast self-examination among market women in Abakaliki, South East Nigeria. Ann Med Health Sci Res 2013;3:7-12.
Bello TO, Olugbenga-Bello AI, Oguntola AS, Adeoti ML, Ojemakinde OM. Knowledge and practice of breast cancer screening among female nurses and lay women in Osogbo, Nigeria. West Afr J Med 2011;30:296-300.
Brandal HB. Diagnostic breast imaging; mammography, sonography, MRI and interventional procedures. Acta Radiol 2015;56:NP21.
Hamisa M, Dabess N, Yosef R, Zakeria F, Hammed Q. Role of breast ultrasound, mammography, magnetic resonance imaging and diffusion weighted imaging in predicting pathologic response of breast cancer after neoadjuvant chemotherapy. Egypt J Radiol Nucl Med 2015;46:245-57.
Ehsani S, Strigel RM, Pettke E, Wilke L, Tevaarwerk AJ, DeMartini WB, et al.
Screening magnetic resonance imaging recommendations and outcomes in patients at high risk for breast cancer. Breast J 2015;21:246-53.
Kuijs VJ, Moossdorff M, Schipper RJ, Beets-Tan RG, Heuts EM, Keymeulen KB, et al.
The role of MRI in axillary lymph node imaging in breast cancer patients: A systematic review. Insights Imaging 2015;6:203-15.
Ursaru M, Jari I, Negru D, Scripcariu V. Local and distant recurrences – A comparative study on conservative and radical surgery for breast cancer. Chirurgia (Bucur) 2015;110:38-42.
Miller JC. Radiology Rounds Newsletter for Referring Physicians. Vol. 1. Massachusetts General Hospital Department of Radiology; 2003.
Ferrini R, Mannino E, Ramsdell E, Hill L. Screening mammography for breast cancer: American college of preventive medicine practice policy statement. Am J Prev Med 1996;12:340-1.
D'Orsi CJ, Sickles EA, Mendelson EB, Morris EA. ACR BI-RADS ®
mammography. In: ACR BI-RADS ®
Atlas, Breast Imaging Reporting and Data System. Reston, VA: American College of Radiology; 2013.
Mushlin AI, Kouides RW, Shapiro DE. Estimating the accuracy of screening mammography: A meta-analysis. Am J Prev Med 1998;14:143-53.
Bray F, Jemal A, Grey N, Ferlay J, Forman D. Global cancer transitions according to the human development index (2008-2030): A population-based study. Lancet Oncol 2012;13:790-801.
Kolb TM, Lichy J, Newhouse JH. Comparison of the performance of screening mammography, physical examination, and breast US and evaluation of factors that influence them: An analysis of 27,825 patient evaluations. Radiology 2002;225:165-75.
Hendrick RE, Smith RA, Rutledge JH III, Smart CR. Benefits of Screening Mammography in Women aged 40-49 years. A new meta-analysis of randomized Clinical Trials. J Natl Cancer Inst Monogr 1997;22:87-92.
Nyström L, Andersson I, Bjurstam N, Frisell J, Nordenskjöld B, Rutqvist LE. Long-term effects of mammography screening: Updated overview of the Swedish randomised trials. Lancet 2002;359:909-19.
Thorbjarnardottir T, Olafsdottir EJ, Valdimarsdottir UA, Olafsson O, Tryggvadottir L. Oral contraceptives, hormone replacement therapy and breast cancer risk: A cohort study of 16 928 women 48 years and older. Acta Oncol 2014;53:752-8.
Olsen O, Gøtzsche PC. Cochrane review on screening for breast cancer with mammography. Lancet 2001;358:1340-2.
Fletcher SW, Black W, Harris R, Rimer BK, Shapiro S. Report of the International Workshop on Screening for Breast Cancer. J Natl Cancer Inst 1993;85:1644-56.
Smith RA, Taplin SH. Breast cancer in limited resources countries. Early detection and access to care. Breast J 2006;12:16-26.
Bird RE, Wallace TW, Yankaskas BC. Analysis of cancers missed at screening mammography. Radiology 1992;184:613-7.
Green BB, Taplin SH. Breast cancer screening controversies. J Am Board Fam Pract 2003;16:233-41.
Johnson ET. Breast cancer racial differences before age 40 – Implications for screening. J Natl Med Assoc 2002;94:149-56.
Aziz H, Hussain F, Sohn C, Mediavillo R, Saitta A, Hussain A, et al.
Early onset of breast carcinoma in African American women with poor prognostic factors. Am J Clin Oncol 1999;22:436-40.
Mai PL, Wideroff L, Greene MH, Graubard BI. Prevalence of family history of breast, colorectal, prostate, and lung cancer in a population-based study. Public Health Genomics 2010;13:495-503.
Stomper PC, D'Souza DJ, DiNitto PA, Arredondo MA. Analysis of parenchymal density on mammograms in 1353 women 25-79 years old. AJR Am J Roentgenol 1996;167:1261-5.
Smith RA, Saslow D, Sawyer KA, Burke W, Costanza ME, Evans WP 3rd
, et al.
American Cancer Society guidelines for breast cancer screening: Update 2003. CA Cancer J Clin 2003;53:141-69.
Cole P, Mark Elwood J, Kaplan SD. Incidence rates and risk factors of benign breast neoplasms. Am J Epidemiol 1978;108:112-20.
Chinyama CN. Benign Breast Diseases: Radiology, Pathology, Risk Assessment. 1st
ed. Heidelberg: Springer; 2004.
Anderson BO, Yip CH, Ramsey SD, Bengoa R, Braun S, Fitch M, et al.
Breast cancer in limited-resource countries: Health care systems and public policy. Breast J 2006;12 Suppl 1:S54-69.
Vasudev P, Onuma K. Secretory breast carcinoma: Unique, triple-negative carcinoma with a favorable prognosis and characteristic molecular expression. Arch Pathol Lab Med 2011;135:1606-10.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2]