|Year : 2019 | Volume
| Issue : 3 | Page : 876-880
Role of sonography as an adjunct to mammography in women with dense breasts
Mohamed R El Kholy1, Waleed A Mousa1, Nagwan R Mishmisha2
1 Department of Radiology, Faculty of Medicine, Menoufia University, Shebin El Kom, Menoufia, Egypt
2 Department of Radiology, Menouf General Hospital, Menouf, Menoufia, Egypt
|Date of Submission||26-Nov-2017|
|Date of Acceptance||29-Jan-2018|
|Date of Web Publication||17-Oct-2019|
Nagwan R Mishmisha
Department of Radiology, Menouf General Hospital, Menouf, Menoufia 32511
Source of Support: None, Conflict of Interest: None
The aim was to evaluate breast lesions using mammography (MG) and ultrasonography (USG) independently and in combination in women with dense breasts.
Women with dense breasts are at higher risk of developing breast cancer and at greater risk of cancer being not detected because of masking of the radiological signs of cancer by increased density. Therefore, multiple imaging modalities are required. USG is an imaging modality that can overcome limitations of MG and it is important for correct diagnosis.
Materials and methods
Our study was carried out on 100 female patients with dense breast lesions who attended Menouf General Hospital from October 2015 to March 2017. All of them were examined clinically followed by both MG and USG examinations. Then, we compared the findings with pathology results to assess their diagnostic performance.
Of all 100 patients included in this study, the benign lesions were 60, whereas the malignant lesions were 40. Considering, MG had a sensitivity of 40%, a specificity of 93%, a positive predictive value (PPV) of 80%, and a negative predictive value (NPV) of 70%, and ultrasound had a sensitivity of 90%, a specificity of 100%, a PPV of 100%, and a NPV of 94%, and the indices of combined MG with ultrasound revealed sensitivity of 100%, specificity of 93%, PPV of 91%, and NPV of 100%.
USG should be considered as an important screening and diagnostic adjunct to MG to minimize the chances of missing diagnosis of any dense breast lesions.
Keywords: breast density, breast neoplasms, mammography, ultrasonography
|How to cite this article:|
El Kholy MR, Mousa WA, Mishmisha NR. Role of sonography as an adjunct to mammography in women with dense breasts. Menoufia Med J 2019;32:876-80
|How to cite this URL:|
El Kholy MR, Mousa WA, Mishmisha NR. Role of sonography as an adjunct to mammography in women with dense breasts. Menoufia Med J [serial online] 2019 [cited 2021 Aug 4];32:876-80. Available from: http://www.mmj.eg.net/text.asp?2019/32/3/876/268854
| Introduction|| |
We evaluated the density of breast parenchyma according to the gradation of the American College of Radiology (ACR) BI-RADS protocol on a scale of A–D, with D representing 'extremely dense breast tissue', denoting that breasts tissue have only glandular tissue with no fatty tissue which could obscure a lesion on mammography (MG); C representing breast tissue that is 'heterogeneously dense', denoting that breasts have mixed fatty tissue with fibroglandular tissue, which may decrease the sensitivity of MG; B representing the presence of 'scattered fibroglandular density', denoting that breasts have increased fatty tissues with scattered mammary parenchyma through all breast tissue; and A representing 'fatty breasts', denoting that the entire breast was replaced by fat .
Around the world, breast malignancy is the most widely recognized type of malignancy and the most common cause of cancer-related death among females. It accounts for 29% of the novel cases of cancer and 15% of cancer-related death and is the second most common cause of cancer-specific death .
Detection of breast cancer in early stages is the critical goal in breast imaging. Breast imaging mainly includes MG and ultrasonography (USG) followed by a biopsy. The mortality of breast cancer can be reduced by the routine screening of healthy women with MG. This is because of changes in the breast like a distortion of fibroglandular architecture asymmetry, neodensity, and microcalcifications, which are picked up earlier than lesions that become clinically palpable or are sometimes detected by self-examination .
The MG occult lesions are usually discovered by clinical examination and usually occur in women who have dense breasts on the mammogram. Therefore, a negative MG result cannot exclude malignancy in women with a palpable mass and the lesion should be biopsied if clinically indicated .
The sonographic evaluation of a palpable breast mass is based on three categories. First, if the lesion is a simple cyst, no further workup is required. However, aspiration can be performed if the patient or physician wants that. Second, for a palpable solid mass or complex cyst, further intervention is often required, such as fine-core cut biopsy. Third, if findings from the sonography are negative (no cystic or solid lesions are seen to be compared with the palpable mass) and the findings from the MG are negative, then the treatment of the abnormal palpable lesion is based on the results of the physical examination .
The aim of our study was to evaluate breast lesions using MG and USG independently and in combination in women with dense breasts.
| Materials and Methods|| |
After approval of the Local Institutional Ethical Committee of Menouf General Hospital and obtaining written consents from all patients to participate in our study, our study was carried out on 100 female patients with dense breast lesions who attended Menouf General Hospital during the period from October 2015 to March 2017. Their age ranged from 30 to 60 years (mean: 38 years).
Inclusion criteria included patients older than 25 years with any breast lesion.
Exclusion criteria included women younger than 25 years, pregnant women, or lactating women.
All of the patients underwent the following procedures: clinical examination including full history taking and physical examination, and then all patients were examined first by a digital mammogram which could classify breast density according to the ACR (A = predominantly fat, B = fat with some fibroglandular tissue, C = heterogeneously dense, and D = extremely dense). Patients who were classified to ACR C and D were then examined by conventional B-mode ultrasound (US). The radiological findings were confirmed by fine needle aspiration cytology (FNAC), core biopsy, or closed follow-up.
Digital MG was performed for each patient using Senographe Essential (GE Healthcare, Wauwatosa, Wisconsin, USA). The patients were exposed to kilovoltage of approximately 28–30 kVp and milliamperage of approximately 30–80 mAs. The examinations were performed based on the standard craniocaudal and mediolateral oblique projections of each breast.
Conventional US was performed by using an annular array mechanical sector scanner with a frequency of 7.5-mHz liner probe (LOGIQ P5; GE Healthcare). Every patient was examined in supine and oblique positions, with the examined side elevated, and the ipsilateral arm was extended behind the head to fix the breast against the chest wall. In few cases, patients were examined in the sitting position when the mass was palpated only in this position. An US gel was applied to the skin of the breast. Each breast was examined quadrant by quadrant starting by the upper inner quadrant of the breast moved laterally to the outer quadrant; this was reported in the same way of the lower quadrants, and then both axillary regions were examined.
According to MG and US diagnosis, 44 patients who had galactocele, fibroadenomat a, fibroadenosis, or fibrocystic disease were finally diagnosed by close follow-up, 12 patients who had cystic lesions as simple cyst and abscesses were finally diagnosed by FNAC, and 44 patients who had solid breast lesions as intraductal carcinoma in situ, invasive duct carcinoma, or intralobular carcinoma were finally diagnosed by core cut biopsy. A total of 12 patients underwent breast operation after diagnosis by core cut biopsy and histopathology correlation, and 28 patients had chemotherapy before operation.
Data were collected, formulated, and statistically analyzed using SPSS version 20 (SPSS Inc., Chicago, Illinois, USA). Categorical data were presented as number and percentages, whereas quantitative data were expressed as mean ± SD and range.
| Results|| |
This study included 100 patients with 92 breast lesions: 80 patients with single lesions, 12 patients with multiple lesions, and eight patients with nonmass lesions.
In this study, the age mean was 38 ± 7.40. According to the ACR BI-RADS lexicon classification, 68/100 (68%) cases were assigned an ACR score of C and 32/100 (32%) cases were assigned an ACR score of D.
Within the 'benign lesions' group, 13.3% were abscess, 6.7% were simple cysts, 33.3% were fibroadenoma, 13.3% were multiple fibroadenomata, 6.7% were fibroadenosis, 13.3% were fibrocystic, 6.7% were galactocele, and 6.7% were phylloid [Figure 1]. However, within the 'malignant lesions' group, 10% were intralobular carcinoma, 70% were invasive duct carcinoma, and 20% were intraductal carcinoma in situ [Figure 2].
|Figure 1: A 36-year-old female patient (a: craniocaudal view, b: mediolateral oblique view) who underwent digital mammography revealed breast density American College of Radiology scale C with upper outer quadrant well-defined rounded hyperdense homogenous mass in the left breast with multiple axillary benign looking lymph nodes (BI-RADS III). (c) Gray-scale ultrasound revealed well-defined oval-shaped mass with heterogeneous echogenicity (BI-RADS III). This mass was considered as benign owing to mammography and sonographic features and was diagnosed as a phylloid tumor on histopathological evaluation.|
Click here to view
|Figure 2: A 32-year-old female patient (a: mediolateral oblique view, b: craniocaudal view) who underwent digital mammography revealed breast density normal mammographic appearance with oval-shaped multiple axillary lymph nodes (BI-RADS II). (c) Gray-scale ultrasound revealed ill-defined hypoechoic mass with irregular shape (BI-RADS V). This mass was considered as malignant owing to sonographic features and was diagnosed as ductal carcinoma in situ on histopathological evaluation.|
Click here to view
On correlating the MG findings with the final diagnoses, 16 lesions were true positives, four lesions were false positive, 24 lesions were false negatives, and 56 lesions were true negatives, so MG had a sensitivity of 40%, a specificity of 93%, a positive predictive value (PPV) of 80%, a negative predictive value (NPV) of 70%, and diagnostic accuracy of 72% [Table 1].
|Table 1: Sensitivity, specificity, positive predictive value, and negative predictive value of mammography, ultrasonography, and combined mammography and ultrasonography|
Click here to view
On correlating the US findings with the final diagnosis, 36 lesions were true positives, 0 lesions were false positive, four lesions were false negatives, and 60 lesions were true negatives, so US had a sensitivity of 90%, a specificity of 100%, a PPV of 100%, a NPV of 94%, and diagnostic accuracy of 96% [Table 1].
Finally, the diagnostic indices of combined MG with breast US revealed sensitivity of 100%, specificity of 93%, PPV of 91% NPV of 100%, and accuracy of 96% [Table 1].
On correlation of final diagnosis with either histological analysis of biopsy samples, FNAC, or close follow-up. The 'benign lesions' group included 60/100 (60%) lesions whereas the 'malignant lesions' group included 40/100 (40%) lesions.
| Discussion|| |
Breast cancer remains one of the most leading causes of death in women older than 40 years . Therefore, diagnosis of breast carcinoma can be complex and needs multiple imaging modalities .
The aim of our study was to study the effect of digital MG and breast USG in the detection and diagnosis of mass lesions in the dense breasts.
In this study, the mean age of the studied group was 38 years, so MG results might not be significant in this population, because MG has limitations in detection of cancer in the dense breast tissue, most commonly of young patients. The younger women tend to have dense breast tissue and numerous milk glands, making cancer detection with MG difficult. To overcome this limitation, additional imaging modality is often needed for sound diagnosis .
Consequently, it has been proved earlier that sonography is more effective for women younger than 35 years and denser breast parenchyma . This is in line with Khan et al.  who included 32% of women with age less than 40 years. Moreover, the same was found in the study conducted by Masroor et al.  where mean age of the studied group was 42 ± 7.33 years (range: 35–65 years).
The most common malignancy was invasive ductal carcinoma, which accounted for 70% (n = 28) of histopathological examination results obtained. Moreover, Okello et al.  reported that the most common malignancy was invasive ductal carcinoma which accounted for 54.5% (n = 12). In addition, this histopathological finding confers with the previous studies of Hong et al.  and Sseggwanyi et al. .
In this study, US detected 36% of the malignant lesions; however, MG detected only 28% of the malignant lesions. This is in line with Okello et al.  who found that US scan detected 27% more malignant lesions than MG did.
This study reported that sensitivity of MG was 40%, which is similar to Sardanelli et al.  who found that sensitivity of MG was 50%. Moreover, the results regarding MG sensitivity were similar to those reported byHoussami et al.  who found that sensitivity of film MG was 69.2% in women aged between 36 and 40 years. However, it was lower than that reported by Malur et al.  who found that the sensitivity of MG as 83.7%. Moreover, it was also lower than Redmond et al.  who found the sensitivity of digital MG for breast cancer to be 87.5%.
The sensitivity of USG in this study was 90%, which is in line with Redmond et al.  whose result regarding USG sensitivity was 95%, and it was also similar to Houssami et al. , who found that sensitivity of USG was 84.6% in women aged between 36 and 40 years.
Specificity of MG in this study was 93% and US was 100%. This is in line with the results of four clinical trials that reported sensitivity of MG to be 93–99% (Warner et al.  and Kriege et al. ) and US to be 88–96% (Sardanelli et al.  and Weinstein et al. ).
This study reported that the sensitivity of USG at 90% was higher than that of film MG at 40%. This is in line with Houssami et al.  who reported that USG had sensitivity of 84.6% and a film MG had sensitivity of 69.2%, in women aged between 36 and 40 years.
Results of this study show that combining both MG and US has a greater sensitivity (100%) than either sonography (90%) or MG (40%) alone. This is in agreement with Alshayookh et al.  who show that combining both MG and US has a greater sensitivity (96%) than either sonography (81.7%) or MG (75.8%) alone.
Moreover, Chae et al.  showed significantly higher sensitivity at 100% for US combined with MG compared with MG alone (54%).
In this work, the diagnostic indices of combined MG with breast US revealed sensitivity of 100%, specificity of 93%, and NPV of 100%. This is in agreement with Masroor et al.  who calculated sensitivity, specificity, and NPV of sonography as a complement to MG to be 100, 85, and 86%, respectively. However, the PPV in this study was 91%, which is higher than that reported by Masroor et al.  who found PPV to be 14%.
The diagnostic indices of combined MG with breast US slightly was slightly higher than a study by Khan et al. , which indicated sensitivity and specificity of combined MG and US as 94.67 and 77.78%, respectively, and was also higher than Moss et al.  who reported sensitivity and specificity of combined MG and US as 94.2 and 67.9%, respectively.
| Conclusion|| |
MG can stratify breast density to dense and nondense. However, USG should be considered as an important screening and diagnostic adjunct to MG to minimize the chances of missing diagnosis of any dense breast lesions.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
American College of Radiology. ACR practice guideline for the performance of screening and diagnostic mammography. American College of Radiology; 2013.
Abd Aziz KK, Tawfik EA, Shaltout EA, Mohamed Abdel Moneum RA. Clinical outcome and survival of breast cancer patients treated at the Clinical Oncology Department, Menoufia University. Menoufia Med J 2015; 28
Morris KT, Vetto JT, Petty JK, Lum SS, Schmidt WA, Toth-Fejel S, et al
. A new score for the evaluation of palpable breast masses in women under age 40. Am J Surg 2002; 184
Kopans DB. Breast imaging
. Philadelphia: Lippincott; 2002. 29-54.
Yang T, Liang H, Chouc C, Huang J, Pan H. Adjunctive digital breast tomosynthesis in diagnosis of breast cancer. Biomed Res Int 2013; 2013
Sleeba T, Subapradha A, Ramachandran M, Krishnaswami M. Role of dual-energy contrast-enhanced digital mammography as a problem-solving tool in dense breasts: a case report. Indian J Radiol Imaging 2013; 23
Khan TS, Malik N, Ishtiaq M, Rashid T. Role of ultrasound as an adjunct modality to mammography in the diagnostic evaluation of breast cancer. J Rawal Med Coll 2016; 20
Bassett LW, Ysrael M, Gold RH, Ysrael C. Usefulness of mammography and sonography in women less than 35 years of age. Radiology 1991; 180
Masroor I, Ahmed M, Pasha S. To evaluate the role of sonography as an adjunct to mammography women with dense breasts. J Pak Med Assoc 2009; 59
Okello J, Kisembo H, Bugeza S, Galukande M. Breast cancer detection using sonography in women with mammographically dense breasts. BMC Med Imaging 2014; 14
Hong AS, Rosen EL, Soo MS, Baker JA. BI-RADS for sonography: positive and negative predictive values of sonographic features. Am J Roentgenol 2005; 184
Sseggwanyi J, Galukande M, Fualal J, Jombwe J. Prevalence of HIV/AIDS among breast cancer patients and the associated clinico-pathological features. Ann Afr Surg 2011; 8
Sardanelli F, Podo F, Santoro F, Manoukian S, Bergonzi S, Trecate G, et al
. Multicenter surveillance of women at high genetic breast cancer risk using mammography, ultrasonography, and contrast-enhanced magnetic resonance imaging (the high breast cancer risk italian 1 study): final results. Invest Radiol 2011; 46
Houssami N, Irwig L, Simpson JM, Mckessar M, Blome S, Noakes J. Sydney breast imaging accuracy study: comparative sensitivity and specificity of mammography and sonography in young women with symptoms. Am J Roentgenol 2003; 180
Malur S, Wurdinger S, Moritz A, Michels W, Schneider A. Comparison of written reports of mammography, sonography and magnetic resonance mammography for preoperative evaluation of breast lesions, with special emphasis on magnetic resonance mammography. Breast Cancer Res 2011; 3
Redmond CE, Healy GM, Murphy CF, Foster A. The use of ultrasonography and digital mammography in women under 40 years with symptomatic breast cancer: a 7-year Irish experience. Ir J Med Sci 2017; 186
Warner E, Plewes DB, Hill KA, Causer PA, Zubovits JT, Jong RA, et al
. Surveillance of BRCA1 and BRCA2 mutation carriers with magnetic resonance imaging, ultrasound, mammography, and clinical breast examination. JAMA 2004; 292
Kriege M, Brekelmans C, Boetes C, Besnard PE, Zonderland HM, Obdeijn IM, et al
. Efficacy of MRI and mammography for breast cancer screening in women with a familial or genetic predisposition. N Engl J Med 2004; 351
Sardanelli F, Podo F, D'Agnolo G, Verdecchia A, Santaquilani M, Musumeci R, et al
. Multicenter comparative multimodality surveillance of women at genetic-familial high risk for breast cancer (HIBCRIT study): interim results. Radiology 2007; 242
Weinstein SP, Localio AR, Conant EF, Rosen M, Thomas KM, Schnall MD. Multimodality screening of high-risk women: a prospective cohort study. J Clin Oncol 2009; 27
Alshayookh FS, Ahmed HM, Awad IA, Jastaniah SD. Ultrasound alongside with mammogram in women with physically dense breast. Adv Breast Cancer Res 2014; 3
Chae EY, Kim HH, Cha JH, Shin HJ, Kim H. Evaluation of screening whole-breast sonography as a supplemental tool in conjunction with mammography in women with dense breasts. J Ultrasound Med 2013; 32
Moss HA, Britton PD, Flower CD, Freeman AH, Lomas DJ, Warren RM. How reliable is modern breast imaging in differentiating benign from malignant breast lesions in the symptomatic population? Clin Radiol 1999; 54
[Figure 1], [Figure 2]