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Mammographic Breast Density Patterns in Asymptomatic Mexican Women

Mammographic Breast Density Patterns in Asymptomatic Mexican Women Hindawi Publishing Corporation Radiology Research and Practice Volume 2012, Article ID 127485, 7 pages doi:10.1155/2012/127485 Clinical Study Mammographic Breast Density Patterns in Asymptomatic Mexican Women 1 2 Ana Laura Calderon-Gar ´ ciduenas, ˜ Monica ´ Sanabria-Mondragon, ´ 3 1 4 Lourdes Hernandez-B ´ eltran, ´ NoeL ´ op ´ ez-Amador, and Ricardo M. Cerda-Flores Instituto de Medicina Forense, Universidad Veracruzana, 94294 Boca del R´ıo, VER, Mexico Unidad de Medicina Familiar No. 2, Instituto Mexicano del Seguro Social, 43612 Tulancingo, HGO, Mexico Centro Medico Nacional del Noreste, Instituto Mexicano del Seguro Social, UMAE 25, 64180 Monterrey, NL, Mexico Facultad de Enfermeria, Universidad Autonoma de Nuevo Leon, 64460 Monterrey, NL, Mexico Correspondence should be addressed to Ana Laura Calderon-Gar ´ ciduenas, ˜ acald911@hotmail.com Received 28 September 2012; Revised 28 November 2012; Accepted 12 December 2012 Academic Editor: Philippe Soyer Copyright © 2012 Ana Laura Calderon-Gar ´ ciduenas ˜ et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Breast density (BD) is a risk factor for breast cancer. Aims. To describe BD patterns in asymptomatic Mexican women and the pathological mammographic findings. Methods and Material. Prospective, descriptive, and comparative study. Women answered a questionnaire and their mammograms were analyzed according to BI-RADS. Univariate (χ ) and conditional logistic regression analyses were performed. Results. In 300 women studied the BD patterns were fat 56.7% (170), fibroglandular 29% (87), heterogeneously dense 5.7% (17), and dense pattern 8.6% (26). Prevalence of fat pattern was significantly different in women under 50 years (37.6%, 44/117) and older than 50 (68.8%, 126/183). Patterns of high breast density (BD) (dense + heterogeneously dense) were observed in 25.6% (30/117) of women ≤50 years and 7.1% (13/183) of women >50. Asymmetry in BD was observed in 22% (66/300). Compression cone ruled out underlying disease in 56 cases. In the remaining 10, biopsy revealed one fibroadenoma, one complex cyst, and 6 invasive and 2 intraductal carcinomas. 2.6% (8/300) of patients had non-palpable carcinomas. Benign lesions were observed in 63.3% (190/300) of cases, vascular calcification in 150 cases (78.9%), and fat necrosis in 38 cases (20%). Conclusions. Mexican women have a low percentage of high-density patterns. 1. Introduction Incidence of BC increases with age. In Mexico, 46% of BC cases occur before age 50 and the age group most affected Breast cancer (BC) is a world health problem. Since 2006, is that between 40 and 49 years [5]. This contrasts with the it is the first neoplasm mortality cause in adult women in United States, where the average age of presentation is 61 Mexico [1]. In 1990, 6000 new cases were registered and by years [6] and with European countries where the incidence 2020, 16,500 are expected. At present, most of these cases is higher in postmenopausal women [6–8]. Mexico’s first are detected by self-exam and only 10% are identified in voluntary mammography screening program was organized stage I [1, 2]. An essential tool in early detection of BC by the Mexican Foundation for Education in Prevention and is mammography. The advance of technology has refined Opportune Detection of Breast Cancer (FUCAM) and the the images with increased accuracy for detecting non-pal- Mexico City Government. It targeted women over 40. More pable lesions [3]. In Mexico, there is a limited number of than 96,000 mammograms were performed in mobile units mammography machines (4 per million population), below for residents in Mexico City’s Federal District over a 22- the OECD (Organisation for Economic Cooperation and month period ending in December 2006. Out of 949 women Development) indicators (19.9 per million population) and with abnormal mammograms, 208 had breast cancer, a rate far from developed countries (France, 42.2/million) [4]. of 2.1%. Most were in situ, stage I (29.4%) or stage II 2 Radiology Research and Practice (42.2%). One percent were in BI-RADS 0, 4, or 5. Of the women diagnosed with cancer, 68.5% were younger than 60, with an average age of 53.5 [9]. Thirty-eight percent of the cancers occurred in women aged 49 or younger [9]. The screening programs are regulated by the Mexican Official Standard (NOM-041-SSA2-2002) [10]. The NOM provides detection through self-examination, clinical exami- nation, and mammography, the latter every one or two years in women 40 to 49 years with two or more risk factors, and annually for all women 50 years, whenever there is a resort [10]. Actually, the program currently covers 19% of the female population aged 40 or more [10]. Mammography is considered the most sensitive tool for detecting early neoplasia. A particular parameter analyzed in mammography is breast density. Mammographic density (a) (b) reflects variations in adipose, stromal, and epithelial tissues [11], associated with advancing age and hormonal changes experienced by the woman. Hence, it is an important para- meter to evaluate and in fact, a risk factor for BC [12]. In the mammary gland, the older the woman, the higher fat content to be found. However, patterns at high risk of cancer have different distributions in different ages and populations. Breast density has the potential to be an important adjunct to risk estimation and to monitor interventions for breast cancer prevention with hormone replacement therapy and by change in life style behaviours [12]. Therefore, the aim of this study is to determine the breast density (BD) patterns in a sample of asymptomatic Mexican women. 2. Material and Methods (c) (d) The hospital is a referral center for cancer patients and is Figure 1: Breast density patterns according to percentage of a training center for radiologists in mammography. The glandular component: (a) fat (up 25%), (b) fibroglandular (25– hospital supports some primary care clinics with mammo- 50%), (c) heterogeneously dense (50–75%), and (d) dense (over grams (medical and educational purposes). Women from 75%). these clinics were recruited for the study. Upon approval by the Research and Ethics Committees, all consecutive women clinically asymptomatic in relation to breast disease who The BD was classified according to the percentage of attended the Department of Radiology and Image (July 2009 glandular component (Figure 1): fat (up 25%), fibrogland- to July 2010) as part of the program of Screening for Cancer ular (25–50%), heterogeneously dense (50–75%), and dense were included in the study. The selection criteria were 40 (over 75%). For statistical evaluation purpose, fat and fibrog- years of age or older, clinically asymptomatic in relation to landular density patterns were considered “low density,” breast disease, sent for early detection of cancer, and who had whereas heterogeneously dense and dense patterns were not had previous malignant breast disease. Exclusion criteria considered “high density.” included the refusal to sign the consent form, no time to The technical quality of mammography was assessed at answer the questionnaire, prior history of breast malignancy, the time of the study [14] and mammary ultrasound (US) or breast resection surgery. was performed if required. US was used as an adjunct to The patients signed informed consent, underwent mam- mammography, when the tissue was very dense, or because mography, and gave the required clinical information based in the presence of a nodule, it was required to know whether on a questionnaire that was conducted in the visit for mam- the content was liquid or solid, also in cases of focal or mography. Mammography studies were analyzed according global asymmetry, to rule out an underlying lesion not to the criteria of BI-RADS [13]. visible by mammography. Mammographic findings were Becauseofthe agedifference in presentation of breast assessed by two radiologists. In cases where classification cancer in Mexico in relation to other countries, we evaluated and/or diagnosis were discordant, another radiologist eval- two groups, women 50 years or younger and women older uated independently the case and afterwards, the study than 50 years (> and <50 years) [5]. was reviewed together to reach an agreement and a final Radiology Research and Practice 3 Table 1: Body mass index (BMI) in 300 Mexican women. the two groups in relation to family history of breast cancer in general, or in first-degree relatives (mother and sisters). BMI Frequency Percentage As expected, menopause was present in less than 50% of Normal (18.5–24.9) 43 14.3% women aged 50 years or younger and in 93% in older women. Overweight (25–29.9) 96 32.0% Women in the north of the country have the highest rate of Grade 1 (30–34.9) 110 36.7% caesarean sections in Mexico, a phenomenon that has already Grade 2 (35–39.9) 37 12.3% been detected since several years ago. Table 3 shows the distribution of BD patterns according Grade 3 (≥40 kg/m)14 4.7% to age. The general distribution of mammographic density Total 300 100% in these women according to BI-RADS classification showed a fat pattern in 56.7% of cases, 29% with fibroglandular pattern, 5.7% with heterogeneous pattern, and 8.6% with consensus was obtained. Benign and malignant findings were high density pattern. described. We used a General Electric digital mammography, Table 4 shows BD and its relationship to women older Senographe Model 2002, and two ultrasound machines and younger than 50 years. Mammographic density was Brand General Electric (model LOGIC 5, 2002, LOGIC strongly influenced by the age of the patient, with significant 7.2003). The ultrasound machines were equipped with difference in younger and older than 50 years. Thus, the 7 MHz linear transducers and 3.5 MHz convex transducer. distribution of the four patterns, fat, fibroglandular, hetero- 19 variables were studied; 15 corresponded to the ques- geneous dense, and dense was 37.6, 36.7, 9.4, and 16.2%, tionnaire: degree of obesity (according to Body Mass Index), respectively, for women under age 50 and 68.8, 24, 3.3 and age of menarche and menopause, tobacco (at least one 3.8% for women over 50 years. cigarette per day) and alcohol consumption (at least one 66 women (22%) showed asymmetry in mammographic drink per week), contraceptive use (type and duration of density. The compression cone ruled out the underlying use), hormone replacement therapy, number of pregnancies, pathology in 56 cases. In the remaining 10 women, lesions cesarean sections and abortions, age and duration of the first were detected that were confirmed by biopsy. These lesions lactation, history of mammography, who requested the study were diagnosed as fibroadenoma (1 case), complex cyst (1 and family history of breast cancer, and 4 mammographic case), and cancer (8 patients). Of the cancers found, 6 features (BD, BI-RADS and pathological findings, benign were invasive ductal carcinomas and 2 were intraductal neo- and malignant). Measurements of weight, height, waist, and plasms. All carcinomas were non-palpable lesions. Cancer hip were made in each patient. was detected in 2.6% of patients in this study. 50% (N = 4) We performed univariate analysis (Chi-square tables) of cancers were found in patients 50 years or younger. and multivariate (conditional logistic regression) using SPSS Of the total sample, 190 women (63.3%) had benign 17. Breast density was studied (1 high and 0 low) as well as lesions that corresponded to vascular calcifications (150 its association with risk factors for breast cancer. The findings patients), fat necrosis (38 patients), and hamartomas (2 were compared in women younger and older than 50 years. patients). 246 cases (82%) only needed the mammography for diagnosis, whereas in 54 patients (18%) it was necessary to supplement the study with ultrasound. 3. Results Mammography identified BI-RADS 1 in 78 patients Of the 362 patients studied, 62 of them were excluded (26%) of which only one required an additional ultrasono- because they refused to sign the consent form (10/62, 16.1%), graphy (US) to define the diagnosis (0.3%); BI-RADS 2 was they had no time to answer the questionnaire (48/62, 77.4%), diagnosed in 190 patients (63.3%) of which the mammo- or there was a prior history of breast resection surgery (4/62, graphy was supplemented with US in 33 patients (11%). 6.4%). The study group was 300 women with age ranging BI-RADS 3 was found in 16 patients, 2 hamartomas and from 40 to 77 years. Significant differences between the two 2 fibroadenomas, the remaining 12 patients needed to groups were not observed in obesity degree (Tables 1 and 2), complement with US, detecting 5 simple cysts, 6 complex age of menarche (≤50: 12.68 ± 1.61; >50: 13.12 ± 1.64, t- cysts and 1 cancer, BI-RADS 4 were 8 cases, and all requir- student −2.305, P = 0.022) tobacco and alcohol consump- ed US complement; findings included 1 complex cyst, 1 tion, history of oral contraceptive use, history of pregnancies fibroadenoma, and 6 neoplastic tumors. and abortions, lactation history, and familial history of BC Cancers detected by both mammography and US were (Table 2). No woman in the study was classified with abuse later corroborated by biopsy. Of these, one was BIRAD 3, problem or alcohol dependency. Less than 20% of women six had BI-RADS 4, and one was BI-RADS 5. Neoplastic were smoking, with an average of 5 cigarettes per day, ±2. cases were associated with fibroglandular density pattern in In these women aged 40 years or older, the present study 3 cases, 3 had heterogeneous, and 2 high-density patterns. was the first to be performed in 40% of cases. The average 5 carcinomas were found in 43 patients with high-density pattern (heterogeneous + dense) and 3 neoplasms were age of the first mammogram was 49.9 years, ranging from 40 to 71 years. The decision to seek mammography performed detected in 3/257 patients with low-density patterns (fat & was the idea of the patient at 7% of cases and it was indicated fibroglandular) (Table 5). Table 5 shows the BI-RADS diag- nosis according to BD patterns. Only dense density pattern by the physician or a nurse as part of the breast cancer screening program in 93%. There was no difference between in this sample was associated to BI-RADS 0. Also, it had the 4 Radiology Research and Practice Table 2: Distribution of characteristics according to age. Age Characteristic χ Probability P ≤50 (117) >50 (183) Normal weight 18 (15.4) 25 (13.7) 0.17 0.678 Overweight-obesity 99 (84.6) 158 (86.3) Menopause No 60 (51.3) 13 (7.1) 75.65 0.000 Yes 57 (48.7) 170 (92.9) Smoker No 98 (83.8) 151 (82.5) 0.08 0.779 Yes 19 (16.2) 32 (17.5) Alcohol consumption No 93 (79.5) 144 (78.7) 0.03 0.868 Yes 24 (20.5) 39 (21.3) History of oral contraceptives No 73 (62.4) 144 (66.7) 0.57 0.449 Yes 24 (37.6) 39 (33.3) Pregnancies No 10 (8.5) 12 (6.6) 0.42 0.519 Yes 107 (91.5) 171 (93.4) Cesarean section No 65 (55.6) 123 (67.2) 4.15 0.042 Yes 52 (44.4) 60 (32.7) Abortion No 90 (76.9) 122 (66.7) 3.62 0.057 Yes 27 (23.1) 61 (33.3) History of lactation No 21 (17.9) 27 (14.8) 0.54 0.462 Yes 96 (82.1) 156 (85.2) Previous mammography No 44 (37.6) 76 (41.5) 0.46 0.499 Yes 73 (62.4) 107 (58.5) Mammography required by: Physician 83 (70.9) 133 (72.7) 0.71 0.702 Nurse (early detection program) 24 (20.5) 39 (21.3) Women 10 (8.5) 11 (6.0) Breast cancer in the family No 86 (73.5) 150 (82.0) 3.05 0.081 Yes 31 (26.5) 33 (18.0) Mother with BC No 112 (95.7) 179 (97.8) 1.07 0.301 Yes 5 (4.3) 4 (2.2) Sister with BC No 107 (91.5) 175 (95.6) 2.21 0.137 Yes 10 (8.5) 8 (4.4) Radiology Research and Practice 5 Table 3: Breast density, and age distribution. Patterns Age (years) Total Fat Fibroglandular Heterogeneously dense Dense 40–45 19 17 7 9 52 46–50 25 26 4 10 65 51–55 53 25 0 3 81 56–60 35 11 3 3 52 61–65 23 4 1 0 28 66–70 11 4 1 0 16 71–77 4 0 1 1 6 Total 170 (56.7%) 87 (29%) 17 (5.7%) 26 (8.6%) Table 4: Breast density in women younger and older than 50 years. ≤50 years >50 years Mammographic density patterns Total n % n % 44 37.6 126 68.8 Fat 170 43 36.7 44 24.0 Fibroglandular 87 11 9.4 6 3.3 Heterogeneously dense 17 19 16.2 7 3.8 Dense 26 Total 117 183 300 χ = 35.5, P = 0.0001, gl = 9. highest proportion of BI-RADS 3 and 4. The cancer cases 8]. Health authorities in Mexico recommend mammography were associated to high density in 5 cases (62.5%). from age 40 if there are at least two risk factors. When compared with other studies, the findings in Mexican women showed particular features. Mammographic 4. Discussion density (percent dense area) was 60% or more in 8.3% of women in the UK [17]. In Korean women [18], the frequency Breast cancer is a major cause of morbidity and mortality of dense mammogram (heterogeneously dense and dense in our country. On the other hand, we have the growing patterns) was 78.3% for women 40−44 years old, 61.1% problem of obesity [15]. Obesity is generally associated with for (45−49) group, and 30.1% in (50−54) age range. In an increased risk of developing breast cancer, which is most Indian population a low prevalence of dense mammographic evident in women with morbid obesity [16]. Only 14% of patterns (16.3% in noncancer controls and 26.7% in breast the women studied were in normal weight and 17% were cancer cases) has been reported [19]. In Western women obese grades III and IV. Age and obesity in women in our figures were 47.2% (40−44 years), 44.8% (45−49), and population were correlated with low-density radiographic 44.4% (50−54) [19]. Mexican women had these frequencies pattern (fat density, 56.7%). However, in spite of obesity 29% of high density, 30.7% (40–45), 21.5% (46–50), and 3.7% of these women had glandular pattern, 5.7% heterogeneous (51–55). Therefore, the percentage of mammary glands with dense pattern, and 8.6% dense pattern. It is this latter group high density was lower than in other countries. of patients in whom the risk of BC is higher. There was The presence of asymmetry in mammographic density a significant difference in the patterns of breast density in requires to rule out underlying breast pathology. Besides women under age 50 as compared with older ones. The additional projections, maximum compression, and lateral fat pattern increased from 38.5% in women under 50 years magnification cone to 90 degrees, the use of ultrasonography to 65.4% in the group of 56–60 years and reached 82% in in our study was very useful to complement the character- women aged 61–65 years. However, even in old age it is ization of lesions of the mammary gland [20]. US helped possible to observe high BD, as the patients in the age group to define diagnosis specially in BI-RADS 3 and 4 in patients of 71–77 years. Breast high density is a risk factor for cancer. with high breast density pattern where the diagnosis included It is known that the incidence of breast cancer increases with simple and complex cysts, fibroadenomas, and cancer. All age. In Mexico, 46% of BC cases occur before age 50 and the patients with a final diagnosis of cancer by mammography age group most affected is that between 40 and 49 years [5]. and ultrasound underwent biopsy to corroborate diagnosis. This contrasts with the United States, where the average age of presentation is 63 years [6, 8] and with European countries Coarse calcifications and fat necrosis were the most where the incidence is higher in postmenopausal women [7, frequent benign lesions in this sample of Mexican women. 6 Radiology Research and Practice Table 5: Distribution of mammographic diagnostics (BI-RADS) according to breast densities patterns. Density pattern BI-RADS Total Fat Fibroglandular Heterogeneously dense Dense BI-RADS 0 0 0 0 7 (26.9%) 7 BI-RADS 1 48 (28.2%) 29 (33.3%) 0 1 (3.8%) 78 BI-RADS 2 116 (68.2%) 51 (58.6%) 13 (76.5%) 10 (38.4%) 190 BI-RADS 3 5 (5.7%) 4 (2.4%) 1 (5.8%) 6 (23%) 16 # carcinomas 1 BI-RADS 4 2 (2.3%) 2 (11.7%) 2 (7.6%) 2 (1.2%) 8 ∗ ∗ ∗ # carcinomas 2 2 2 BI-RADS 5 1 (5.8%) # carcinomas 1 Total 170 (56.6%) 87 (29%) 17 (5.7%) 26 (8.7%) 300 Number of carcinomas. In this sample, 2.6% of patients had non-palpable cancer. [5] S. Rodr´ıguez-Cuevas,C.G.Mac´ıas, D. Franceschi, and S. Labastida, “Breast carcinoma presents a decade earlier in The patients were referred for routine mammography. This Mexican Women than in Women in the United States or finding is similar to the percentage found in the review of European countries,” Cancer, vol. 91, no. 4, pp. 863–868, 2001. 96,000 mammograms in Mexico [9]. Carcinomas in this [6] National Cancer Data Base, American Cancer Society, An- small sample were observed in 11.6% of women with high- nual Review of Patient Care, EUA, Atlanta, Ga, USA, 1993, density patterns, and in 1.1% of patients with low-density http://www.cancer.org/acs/groups/content/@epidemiology- breast pattern, which supports the claim that high breast surveilance/documents/document/acspc-027766.pdf. density is a risk factor for carcinoma. [7] A.H.Olsen,K.Bihrmann, M. B. Jensen,I.Vejborg,and E. Lynge, “Breast density and outcome of mammography screen- ing: a cohort study,” British Journal of Cancer, vol. 100, no. 7, 5. Conclusion pp. 1205–1208, 2009. [8] F. Bray, P. McCarron, and D. M. Parkin, “The changing global In general, Mexican women over 40 years of age have a breast patterns of female breast cancer incidence and mortality,” density profile different from Asian and European women. Breast Cancer Research, vol. 6, no. 6, pp. 229–239, 2004. 25.6% of women under 50 years of age and 7.1% of older [9] S. Rodr´ıguez-Cuevas, F. Guisa-Hohenstein, and S. Labastida- women have high breast density. It would be interesting Almendaro, “First breast cancer mammography screening to compare the BD distribution patterns with other Latin program in Mexico: initial results 2005-2006,” Breast Journal, American populations and determine if they are similar, vol. 15, no. 6, pp. 623–631, 2009. especially due to risk of carcinoma in high breast density [10] NORMA Oficial Mexicana, “Para la prevencion, ´ diagnostic ´ o, patterns. tratamiento, control y vigilancia epidemiolog ´ ica del canc ´ er de mama,” NOM-041-SSA2-2002, http://www.salud.gob.mx/ Acknowledgment unidades/cdi/nom/041ssa202.html. [11] M. J. Yaffe, “Mammographic density. Measurement of mam- The authors appreciate the facilities provided by the Mexican mographic density,” Breast Cancer Research, vol. 10, no. 3, Social Security Institute for carrying out this work. article 209, 2008. [12] A. Manduca, M. J. Carston, J. J. 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Medical technologies,” http:// attributable fractions,” BMC Cancer, vol. 12, no. 1, article 414, bit.ly/ioQzL. 2012. Radiology Research and Practice 7 [17] D. G. Evans, J. Warwick, S. M. Astley et al., “Assessing indi- vidual breast cancer risk within the U.K. National Health Service Breast Screening Program: a new paradigm for cancer prevention,” Cancer Prevention Research, vol. 5, no. 7, pp. 943– 951, 2012. [18] S. H. Kim, M. H. Kim, and K. K. Oh, “Analysis and comparison of breast density according to age on mammogram between Korean and Western women,” TheJournal of theKorean Radiological Society, vol. 42, no. 6, pp. 1009–1014, 2000. [19] A. Attam, N. Kaur, S. Saha, and S. K. Bhargava, “Mammo- graphic density as a risk factor for breast cancer in a low risk population,” Indian Journal of Cancer, vol. 45, no. 2, pp. 50–53, [20] M. Nothacker, V. Duda, M. 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Hindawi Publishing Corporation Radiology Research and Practice Volume 2012, Article ID 127485, 7 pages doi:10.1155/2012/127485 Clinical Study Mammographic Breast Density Patterns in Asymptomatic Mexican Women 1 2 Ana Laura Calderon-Gar ´ ciduenas, ˜ Monica ´ Sanabria-Mondragon, ´ 3 1 4 Lourdes Hernandez-B ´ eltran, ´ NoeL ´ op ´ ez-Amador, and Ricardo M. Cerda-Flores Instituto de Medicina Forense, Universidad Veracruzana, 94294 Boca del R´ıo, VER, Mexico Unidad de Medicina Familiar No. 2, Instituto Mexicano del Seguro Social, 43612 Tulancingo, HGO, Mexico Centro Medico Nacional del Noreste, Instituto Mexicano del Seguro Social, UMAE 25, 64180 Monterrey, NL, Mexico Facultad de Enfermeria, Universidad Autonoma de Nuevo Leon, 64460 Monterrey, NL, Mexico Correspondence should be addressed to Ana Laura Calderon-Gar ´ ciduenas, ˜ acald911@hotmail.com Received 28 September 2012; Revised 28 November 2012; Accepted 12 December 2012 Academic Editor: Philippe Soyer Copyright © 2012 Ana Laura Calderon-Gar ´ ciduenas ˜ et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Breast density (BD) is a risk factor for breast cancer. Aims. To describe BD patterns in asymptomatic Mexican women and the pathological mammographic findings. Methods and Material. Prospective, descriptive, and comparative study. Women answered a questionnaire and their mammograms were analyzed according to BI-RADS. Univariate (χ ) and conditional logistic regression analyses were performed. Results. In 300 women studied the BD patterns were fat 56.7% (170), fibroglandular 29% (87), heterogeneously dense 5.7% (17), and dense pattern 8.6% (26). Prevalence of fat pattern was significantly different in women under 50 years (37.6%, 44/117) and older than 50 (68.8%, 126/183). Patterns of high breast density (BD) (dense + heterogeneously dense) were observed in 25.6% (30/117) of women ≤50 years and 7.1% (13/183) of women >50. Asymmetry in BD was observed in 22% (66/300). Compression cone ruled out underlying disease in 56 cases. In the remaining 10, biopsy revealed one fibroadenoma, one complex cyst, and 6 invasive and 2 intraductal carcinomas. 2.6% (8/300) of patients had non-palpable carcinomas. Benign lesions were observed in 63.3% (190/300) of cases, vascular calcification in 150 cases (78.9%), and fat necrosis in 38 cases (20%). Conclusions. Mexican women have a low percentage of high-density patterns. 1. Introduction Incidence of BC increases with age. In Mexico, 46% of BC cases occur before age 50 and the age group most affected Breast cancer (BC) is a world health problem. Since 2006, is that between 40 and 49 years [5]. This contrasts with the it is the first neoplasm mortality cause in adult women in United States, where the average age of presentation is 61 Mexico [1]. In 1990, 6000 new cases were registered and by years [6] and with European countries where the incidence 2020, 16,500 are expected. At present, most of these cases is higher in postmenopausal women [6–8]. Mexico’s first are detected by self-exam and only 10% are identified in voluntary mammography screening program was organized stage I [1, 2]. An essential tool in early detection of BC by the Mexican Foundation for Education in Prevention and is mammography. The advance of technology has refined Opportune Detection of Breast Cancer (FUCAM) and the the images with increased accuracy for detecting non-pal- Mexico City Government. It targeted women over 40. More pable lesions [3]. In Mexico, there is a limited number of than 96,000 mammograms were performed in mobile units mammography machines (4 per million population), below for residents in Mexico City’s Federal District over a 22- the OECD (Organisation for Economic Cooperation and month period ending in December 2006. Out of 949 women Development) indicators (19.9 per million population) and with abnormal mammograms, 208 had breast cancer, a rate far from developed countries (France, 42.2/million) [4]. of 2.1%. Most were in situ, stage I (29.4%) or stage II 2 Radiology Research and Practice (42.2%). One percent were in BI-RADS 0, 4, or 5. Of the women diagnosed with cancer, 68.5% were younger than 60, with an average age of 53.5 [9]. Thirty-eight percent of the cancers occurred in women aged 49 or younger [9]. The screening programs are regulated by the Mexican Official Standard (NOM-041-SSA2-2002) [10]. The NOM provides detection through self-examination, clinical exami- nation, and mammography, the latter every one or two years in women 40 to 49 years with two or more risk factors, and annually for all women 50 years, whenever there is a resort [10]. Actually, the program currently covers 19% of the female population aged 40 or more [10]. Mammography is considered the most sensitive tool for detecting early neoplasia. A particular parameter analyzed in mammography is breast density. Mammographic density (a) (b) reflects variations in adipose, stromal, and epithelial tissues [11], associated with advancing age and hormonal changes experienced by the woman. Hence, it is an important para- meter to evaluate and in fact, a risk factor for BC [12]. In the mammary gland, the older the woman, the higher fat content to be found. However, patterns at high risk of cancer have different distributions in different ages and populations. Breast density has the potential to be an important adjunct to risk estimation and to monitor interventions for breast cancer prevention with hormone replacement therapy and by change in life style behaviours [12]. Therefore, the aim of this study is to determine the breast density (BD) patterns in a sample of asymptomatic Mexican women. 2. Material and Methods (c) (d) The hospital is a referral center for cancer patients and is Figure 1: Breast density patterns according to percentage of a training center for radiologists in mammography. The glandular component: (a) fat (up 25%), (b) fibroglandular (25– hospital supports some primary care clinics with mammo- 50%), (c) heterogeneously dense (50–75%), and (d) dense (over grams (medical and educational purposes). Women from 75%). these clinics were recruited for the study. Upon approval by the Research and Ethics Committees, all consecutive women clinically asymptomatic in relation to breast disease who The BD was classified according to the percentage of attended the Department of Radiology and Image (July 2009 glandular component (Figure 1): fat (up 25%), fibrogland- to July 2010) as part of the program of Screening for Cancer ular (25–50%), heterogeneously dense (50–75%), and dense were included in the study. The selection criteria were 40 (over 75%). For statistical evaluation purpose, fat and fibrog- years of age or older, clinically asymptomatic in relation to landular density patterns were considered “low density,” breast disease, sent for early detection of cancer, and who had whereas heterogeneously dense and dense patterns were not had previous malignant breast disease. Exclusion criteria considered “high density.” included the refusal to sign the consent form, no time to The technical quality of mammography was assessed at answer the questionnaire, prior history of breast malignancy, the time of the study [14] and mammary ultrasound (US) or breast resection surgery. was performed if required. US was used as an adjunct to The patients signed informed consent, underwent mam- mammography, when the tissue was very dense, or because mography, and gave the required clinical information based in the presence of a nodule, it was required to know whether on a questionnaire that was conducted in the visit for mam- the content was liquid or solid, also in cases of focal or mography. Mammography studies were analyzed according global asymmetry, to rule out an underlying lesion not to the criteria of BI-RADS [13]. visible by mammography. Mammographic findings were Becauseofthe agedifference in presentation of breast assessed by two radiologists. In cases where classification cancer in Mexico in relation to other countries, we evaluated and/or diagnosis were discordant, another radiologist eval- two groups, women 50 years or younger and women older uated independently the case and afterwards, the study than 50 years (> and <50 years) [5]. was reviewed together to reach an agreement and a final Radiology Research and Practice 3 Table 1: Body mass index (BMI) in 300 Mexican women. the two groups in relation to family history of breast cancer in general, or in first-degree relatives (mother and sisters). BMI Frequency Percentage As expected, menopause was present in less than 50% of Normal (18.5–24.9) 43 14.3% women aged 50 years or younger and in 93% in older women. Overweight (25–29.9) 96 32.0% Women in the north of the country have the highest rate of Grade 1 (30–34.9) 110 36.7% caesarean sections in Mexico, a phenomenon that has already Grade 2 (35–39.9) 37 12.3% been detected since several years ago. Table 3 shows the distribution of BD patterns according Grade 3 (≥40 kg/m)14 4.7% to age. The general distribution of mammographic density Total 300 100% in these women according to BI-RADS classification showed a fat pattern in 56.7% of cases, 29% with fibroglandular pattern, 5.7% with heterogeneous pattern, and 8.6% with consensus was obtained. Benign and malignant findings were high density pattern. described. We used a General Electric digital mammography, Table 4 shows BD and its relationship to women older Senographe Model 2002, and two ultrasound machines and younger than 50 years. Mammographic density was Brand General Electric (model LOGIC 5, 2002, LOGIC strongly influenced by the age of the patient, with significant 7.2003). The ultrasound machines were equipped with difference in younger and older than 50 years. Thus, the 7 MHz linear transducers and 3.5 MHz convex transducer. distribution of the four patterns, fat, fibroglandular, hetero- 19 variables were studied; 15 corresponded to the ques- geneous dense, and dense was 37.6, 36.7, 9.4, and 16.2%, tionnaire: degree of obesity (according to Body Mass Index), respectively, for women under age 50 and 68.8, 24, 3.3 and age of menarche and menopause, tobacco (at least one 3.8% for women over 50 years. cigarette per day) and alcohol consumption (at least one 66 women (22%) showed asymmetry in mammographic drink per week), contraceptive use (type and duration of density. The compression cone ruled out the underlying use), hormone replacement therapy, number of pregnancies, pathology in 56 cases. In the remaining 10 women, lesions cesarean sections and abortions, age and duration of the first were detected that were confirmed by biopsy. These lesions lactation, history of mammography, who requested the study were diagnosed as fibroadenoma (1 case), complex cyst (1 and family history of breast cancer, and 4 mammographic case), and cancer (8 patients). Of the cancers found, 6 features (BD, BI-RADS and pathological findings, benign were invasive ductal carcinomas and 2 were intraductal neo- and malignant). Measurements of weight, height, waist, and plasms. All carcinomas were non-palpable lesions. Cancer hip were made in each patient. was detected in 2.6% of patients in this study. 50% (N = 4) We performed univariate analysis (Chi-square tables) of cancers were found in patients 50 years or younger. and multivariate (conditional logistic regression) using SPSS Of the total sample, 190 women (63.3%) had benign 17. Breast density was studied (1 high and 0 low) as well as lesions that corresponded to vascular calcifications (150 its association with risk factors for breast cancer. The findings patients), fat necrosis (38 patients), and hamartomas (2 were compared in women younger and older than 50 years. patients). 246 cases (82%) only needed the mammography for diagnosis, whereas in 54 patients (18%) it was necessary to supplement the study with ultrasound. 3. Results Mammography identified BI-RADS 1 in 78 patients Of the 362 patients studied, 62 of them were excluded (26%) of which only one required an additional ultrasono- because they refused to sign the consent form (10/62, 16.1%), graphy (US) to define the diagnosis (0.3%); BI-RADS 2 was they had no time to answer the questionnaire (48/62, 77.4%), diagnosed in 190 patients (63.3%) of which the mammo- or there was a prior history of breast resection surgery (4/62, graphy was supplemented with US in 33 patients (11%). 6.4%). The study group was 300 women with age ranging BI-RADS 3 was found in 16 patients, 2 hamartomas and from 40 to 77 years. Significant differences between the two 2 fibroadenomas, the remaining 12 patients needed to groups were not observed in obesity degree (Tables 1 and 2), complement with US, detecting 5 simple cysts, 6 complex age of menarche (≤50: 12.68 ± 1.61; >50: 13.12 ± 1.64, t- cysts and 1 cancer, BI-RADS 4 were 8 cases, and all requir- student −2.305, P = 0.022) tobacco and alcohol consump- ed US complement; findings included 1 complex cyst, 1 tion, history of oral contraceptive use, history of pregnancies fibroadenoma, and 6 neoplastic tumors. and abortions, lactation history, and familial history of BC Cancers detected by both mammography and US were (Table 2). No woman in the study was classified with abuse later corroborated by biopsy. Of these, one was BIRAD 3, problem or alcohol dependency. Less than 20% of women six had BI-RADS 4, and one was BI-RADS 5. Neoplastic were smoking, with an average of 5 cigarettes per day, ±2. cases were associated with fibroglandular density pattern in In these women aged 40 years or older, the present study 3 cases, 3 had heterogeneous, and 2 high-density patterns. was the first to be performed in 40% of cases. The average 5 carcinomas were found in 43 patients with high-density pattern (heterogeneous + dense) and 3 neoplasms were age of the first mammogram was 49.9 years, ranging from 40 to 71 years. The decision to seek mammography performed detected in 3/257 patients with low-density patterns (fat & was the idea of the patient at 7% of cases and it was indicated fibroglandular) (Table 5). Table 5 shows the BI-RADS diag- nosis according to BD patterns. Only dense density pattern by the physician or a nurse as part of the breast cancer screening program in 93%. There was no difference between in this sample was associated to BI-RADS 0. Also, it had the 4 Radiology Research and Practice Table 2: Distribution of characteristics according to age. Age Characteristic χ Probability P ≤50 (117) >50 (183) Normal weight 18 (15.4) 25 (13.7) 0.17 0.678 Overweight-obesity 99 (84.6) 158 (86.3) Menopause No 60 (51.3) 13 (7.1) 75.65 0.000 Yes 57 (48.7) 170 (92.9) Smoker No 98 (83.8) 151 (82.5) 0.08 0.779 Yes 19 (16.2) 32 (17.5) Alcohol consumption No 93 (79.5) 144 (78.7) 0.03 0.868 Yes 24 (20.5) 39 (21.3) History of oral contraceptives No 73 (62.4) 144 (66.7) 0.57 0.449 Yes 24 (37.6) 39 (33.3) Pregnancies No 10 (8.5) 12 (6.6) 0.42 0.519 Yes 107 (91.5) 171 (93.4) Cesarean section No 65 (55.6) 123 (67.2) 4.15 0.042 Yes 52 (44.4) 60 (32.7) Abortion No 90 (76.9) 122 (66.7) 3.62 0.057 Yes 27 (23.1) 61 (33.3) History of lactation No 21 (17.9) 27 (14.8) 0.54 0.462 Yes 96 (82.1) 156 (85.2) Previous mammography No 44 (37.6) 76 (41.5) 0.46 0.499 Yes 73 (62.4) 107 (58.5) Mammography required by: Physician 83 (70.9) 133 (72.7) 0.71 0.702 Nurse (early detection program) 24 (20.5) 39 (21.3) Women 10 (8.5) 11 (6.0) Breast cancer in the family No 86 (73.5) 150 (82.0) 3.05 0.081 Yes 31 (26.5) 33 (18.0) Mother with BC No 112 (95.7) 179 (97.8) 1.07 0.301 Yes 5 (4.3) 4 (2.2) Sister with BC No 107 (91.5) 175 (95.6) 2.21 0.137 Yes 10 (8.5) 8 (4.4) Radiology Research and Practice 5 Table 3: Breast density, and age distribution. Patterns Age (years) Total Fat Fibroglandular Heterogeneously dense Dense 40–45 19 17 7 9 52 46–50 25 26 4 10 65 51–55 53 25 0 3 81 56–60 35 11 3 3 52 61–65 23 4 1 0 28 66–70 11 4 1 0 16 71–77 4 0 1 1 6 Total 170 (56.7%) 87 (29%) 17 (5.7%) 26 (8.6%) Table 4: Breast density in women younger and older than 50 years. ≤50 years >50 years Mammographic density patterns Total n % n % 44 37.6 126 68.8 Fat 170 43 36.7 44 24.0 Fibroglandular 87 11 9.4 6 3.3 Heterogeneously dense 17 19 16.2 7 3.8 Dense 26 Total 117 183 300 χ = 35.5, P = 0.0001, gl = 9. highest proportion of BI-RADS 3 and 4. The cancer cases 8]. Health authorities in Mexico recommend mammography were associated to high density in 5 cases (62.5%). from age 40 if there are at least two risk factors. When compared with other studies, the findings in Mexican women showed particular features. Mammographic 4. Discussion density (percent dense area) was 60% or more in 8.3% of women in the UK [17]. In Korean women [18], the frequency Breast cancer is a major cause of morbidity and mortality of dense mammogram (heterogeneously dense and dense in our country. On the other hand, we have the growing patterns) was 78.3% for women 40−44 years old, 61.1% problem of obesity [15]. Obesity is generally associated with for (45−49) group, and 30.1% in (50−54) age range. In an increased risk of developing breast cancer, which is most Indian population a low prevalence of dense mammographic evident in women with morbid obesity [16]. Only 14% of patterns (16.3% in noncancer controls and 26.7% in breast the women studied were in normal weight and 17% were cancer cases) has been reported [19]. In Western women obese grades III and IV. Age and obesity in women in our figures were 47.2% (40−44 years), 44.8% (45−49), and population were correlated with low-density radiographic 44.4% (50−54) [19]. Mexican women had these frequencies pattern (fat density, 56.7%). However, in spite of obesity 29% of high density, 30.7% (40–45), 21.5% (46–50), and 3.7% of these women had glandular pattern, 5.7% heterogeneous (51–55). Therefore, the percentage of mammary glands with dense pattern, and 8.6% dense pattern. It is this latter group high density was lower than in other countries. of patients in whom the risk of BC is higher. There was The presence of asymmetry in mammographic density a significant difference in the patterns of breast density in requires to rule out underlying breast pathology. Besides women under age 50 as compared with older ones. The additional projections, maximum compression, and lateral fat pattern increased from 38.5% in women under 50 years magnification cone to 90 degrees, the use of ultrasonography to 65.4% in the group of 56–60 years and reached 82% in in our study was very useful to complement the character- women aged 61–65 years. However, even in old age it is ization of lesions of the mammary gland [20]. US helped possible to observe high BD, as the patients in the age group to define diagnosis specially in BI-RADS 3 and 4 in patients of 71–77 years. Breast high density is a risk factor for cancer. with high breast density pattern where the diagnosis included It is known that the incidence of breast cancer increases with simple and complex cysts, fibroadenomas, and cancer. All age. In Mexico, 46% of BC cases occur before age 50 and the patients with a final diagnosis of cancer by mammography age group most affected is that between 40 and 49 years [5]. and ultrasound underwent biopsy to corroborate diagnosis. This contrasts with the United States, where the average age of presentation is 63 years [6, 8] and with European countries Coarse calcifications and fat necrosis were the most where the incidence is higher in postmenopausal women [7, frequent benign lesions in this sample of Mexican women. 6 Radiology Research and Practice Table 5: Distribution of mammographic diagnostics (BI-RADS) according to breast densities patterns. Density pattern BI-RADS Total Fat Fibroglandular Heterogeneously dense Dense BI-RADS 0 0 0 0 7 (26.9%) 7 BI-RADS 1 48 (28.2%) 29 (33.3%) 0 1 (3.8%) 78 BI-RADS 2 116 (68.2%) 51 (58.6%) 13 (76.5%) 10 (38.4%) 190 BI-RADS 3 5 (5.7%) 4 (2.4%) 1 (5.8%) 6 (23%) 16 # carcinomas 1 BI-RADS 4 2 (2.3%) 2 (11.7%) 2 (7.6%) 2 (1.2%) 8 ∗ ∗ ∗ # carcinomas 2 2 2 BI-RADS 5 1 (5.8%) # carcinomas 1 Total 170 (56.6%) 87 (29%) 17 (5.7%) 26 (8.7%) 300 Number of carcinomas. In this sample, 2.6% of patients had non-palpable cancer. [5] S. Rodr´ıguez-Cuevas,C.G.Mac´ıas, D. Franceschi, and S. Labastida, “Breast carcinoma presents a decade earlier in The patients were referred for routine mammography. This Mexican Women than in Women in the United States or finding is similar to the percentage found in the review of European countries,” Cancer, vol. 91, no. 4, pp. 863–868, 2001. 96,000 mammograms in Mexico [9]. Carcinomas in this [6] National Cancer Data Base, American Cancer Society, An- small sample were observed in 11.6% of women with high- nual Review of Patient Care, EUA, Atlanta, Ga, USA, 1993, density patterns, and in 1.1% of patients with low-density http://www.cancer.org/acs/groups/content/@epidemiology- breast pattern, which supports the claim that high breast surveilance/documents/document/acspc-027766.pdf. density is a risk factor for carcinoma. [7] A.H.Olsen,K.Bihrmann, M. B. Jensen,I.Vejborg,and E. Lynge, “Breast density and outcome of mammography screen- ing: a cohort study,” British Journal of Cancer, vol. 100, no. 7, 5. Conclusion pp. 1205–1208, 2009. 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