|ORIGINAL RESEARCH REPORT
|Year : 2015 | Volume
| Issue : 1 | Page : 3-8
Ultrasound-guided core biopsy of breast lesions in Ibadan: Our initial experience
Millicent O Obajimi1, Adenike T Adeniji-Sofoluwe1, Temitope O Soyemi1, Abideen O Oluwasola2, Adefemi O Afolabi3, Adewunmi O Adeoye2, Babatunde O Adedokun4, Olushola A Mosuro5, Theresa N Elumelu6, Oku S Bassey1, Oludamilola O Osofundiya1, Abayomi Odetunde7, Doyin Olusunmade1, Chinwe E Ukaigwe1
1 Department of Radiology, College of Medicine, University of Ibadan, Ibadan, Nigeria
2 Department of Pathology, College of Medicine, University of Ibadan, Ibadan, Nigeria
3 Department of Surgery, College of Medicine, University of Ibadan, Ibadan, Nigeria
4 Department of Epidemiology, Medical Statistics and Environmental Health, College of Medicine, University of Ibadan, Ibadan, Nigeria
5 Department of Family Medicine, University College Hospital, Ibadan, Nigeria
6 Department of Radiotherapy, College of Medicine, University of Ibadan, Ibadan, Nigeria
7 Institute of Advanced Medical Research and Training, College of Medicine, University of Ibadan, Ibadan, Nigeria
|Date of Web Publication||14-Jul-2015|
Dr. Adenike T Adeniji-Sofoluwe
Department of Radiology, College of Medicine, University College Hospital, University of Ibadan, Ibadan
Source of Support: None, Conflict of Interest: None
Background and Objectives: Ultrasound-guided core needle or tru-cut biopsy is a new concept in breast cancer diagnosis and treatment in developing countries, including Nigeria. A tru-cut biopsy is less invasive surgery, replacing diagnostic surgical biopsies in many institutions. It has a known sensitivity of 94-100%, whether performed with ultrasound or stereotactic guidance. The technique is reliable, simple, reproducible, and relatively cheap. Aims: This is a premier report of ultrasound- guided core biopsy of the breast in Nigeria. This study will evaluate the sampling adequacy and diagnostic accuracy of sonomammographic-guided tru-cut biopsies in determining the nature of a breast lump sent for histopathological analysis. Materials and Methods: A prospective study involving 40 women with clinical suspicion of breast cancer and/or Breast Imaging-Reporting and Data System (BI-RADS) category 3-5 referred for breast imaging at the Department of Radiology of the University College Hospital, Ibadan. Core biopsy was performed with a manual BARD Magnum™ gun, a General Electric GE Logiq P5 ultrasound unit with a high frequency linear transducer. Statistical Package for social sciences [SPSS] Software version 17.0 was used for statistical analysis. Results: Forty core needle biopsies (CNB) were performed on palpable masses. Histopathology confirmed cancer in 24 (60%), while 10 (25%) were benign. Invasive ductal carcinoma accounted for 88% of cancers. Sensitivity and specificity of the core biopsies was found to be 100% and 80%, respectively. Conclusion: Ultrasound-guided biopsy for breast lesion assessment in our center shows high accuracy in determining the nature of a breast lump. Its routine use in countries with limited resources is recommended.
Keywords: Breast, core needle biopsy, masses,ultrasound
|How to cite this article:|
Obajimi MO, Adeniji-Sofoluwe AT, Soyemi TO, Oluwasola AO, Afolabi AO, Adeoye AO, Adedokun BO, Mosuro OA, Elumelu TN, Bassey OS, Osofundiya OO, Odetunde A, Olusunmade D, Ukaigwe CE. Ultrasound-guided core biopsy of breast lesions in Ibadan: Our initial experience. J Clin Sci 2015;12:3-8
|How to cite this URL:|
Obajimi MO, Adeniji-Sofoluwe AT, Soyemi TO, Oluwasola AO, Afolabi AO, Adeoye AO, Adedokun BO, Mosuro OA, Elumelu TN, Bassey OS, Osofundiya OO, Odetunde A, Olusunmade D, Ukaigwe CE. Ultrasound-guided core biopsy of breast lesions in Ibadan: Our initial experience. J Clin Sci [serial online] 2015 [cited 2019 Aug 19];12:3-8. Available from: http://www.jcsjournal.org/text.asp?2015/12/1/3/160758
| Introduction|| |
Core needle biopsy (CNB) of the breast was first introduced by Ellis and Martin in 1930 in New York for the cytological evaluation of a solid lesion.  Then fine-needle aspiration (FNA) was rapidly disseminated in Europe and the United States as part of a triple assessment of palpable breast lesions. ,
This study evaluates the sampling adequacy of sonographic-guided CNB and diagnostic accuracy of the American College of Radiology (ACR) breast imaging and the Breast Imaging-Reporting and Data System (BI-RADS) assessments of lesions in determining the nature of breast lumps encountered at the University College Hospital, Ibadan, Nigeria.
| Materials and Methods|| |
A prospective and descriptive study was carried out over a four year period (2008-2012) at the departments of Surgery, Pathology, and Breast Unit of the Radiology Department of the University College Hospital Ibadan, in collaboration with affiliate units of the University of Ibadan. A total of 40 women ages 20-69 years old underwent tru-cut biopsies due to clinical suspicion and/or a final ACR B-IRADS category 3-5 at imaging. All lesions were palpable and were well-outlined by sonography utilizing a GE logic P5 ultrasound unit with a high frequency linear transducer. The procedure was performed by two radiologists Millicent Obajimi (MO) and Adenike Temitayo Adeniji-Sofoluwe (ATS) with 3 or 4 passes made using a manual spring-loaded BARD Magnum™ gun [Figure 1] and [Figure 2]. Informed consent was obtained from all participants before imaging and biopsy, and an ethical approval was obtained from the UI/UCH institutional review Committee. Tru-cut specimens were sent to the pathology laboratory for histo-immunochemistry. The specificity, sensitivity, and accuracy of sonomammographic diagnosis were then evaluated with reference to the histopathology reports of the biopsy samples.
|Figure 1: Pre-core biopsy image note: Core biopsy needle on the margin/edge of the mass to be biopsied|
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|Figure 2: Post-core biopsy image showing the core biopsy needle passing through the mass|
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| Results|| |
A total of 40 breast ultrasound-guided CNBs were performed during the 4-year study period. The majority (85%) yielded adequate tissue samples for definitive diagnosis. Five samples had inadequate tissue, while the sixth study was abandoned due to severe haemorrhage, a known complication of the procedure. Women in the 40-49 age group and those less than 40 years were predominant and constituted 29.4% (10) of the study population each (58.8%). The distribution of the final ACR Bi-RADS Category among the 34 patients following breast sonographic imaging is shown on [Table 1]. Suspicious lesions (BI-RADS 4 and 5) were reported in 26 (76.5%) women while ACR BI-RADS 3 was reported in 8 (23.5) women, as depicted in [Figure 3].
|Figure 3: Bar chart showing correlation of ultrasound diagnosis using ACR BI-RADS category with histopathological diagnosis|
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|Table 1: Correlation of ultrasound diagnosis using ACR BI-RADS category and histopathology report |
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At histopathology, 24 (92.3%) of the 26 with BI-RADS 4 category were reported as cancerous, while the remaining two (7.7%) were benign [Table 2]. All the patients with ACR BI-RADS 3 category were confirmed to be benign lesions. Of the 24 malignant lesions, 88% were found to be invasive ductal carcinoma [Figure 4]. Fibrocystic changes was the preponderant BIRADS 3 category finding (60%), [Figure 5] illustrates the spectrum of benign lesions in the study.
|Table 2: Accuracy of ultrasound in predicting the histopathology of breast lesions |
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The results of immuno-chemistry in 15 patients is portrayed in [Figure 6]. Eight (53.3%) were triple-negative, 4 (26.7%) were human epidermal growth factor receptor 2 (HER-2) positive and one each (6.7%) with triple positive, estrogren receptor/progesterone receptor (ER/PR) positive, and PR positive.
|Figure 6: Pattern of distribution of immunochemistry in biopsy specimens|
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| Discussion|| |
The earliest report in the literature for ultrasound -guided breast biopsy was in 1987. Widespread use of this guided biopsy began in the early 2000s in Europe and United States.  In 1996, the National Cancer Institute (NCI) published a guideline for breast FNA interpretation. , However, FNA had its demerits, which include attending difficulty in the interpretation of cytology, which sometimes makes definite diagnosis impossible, sample insufficiency seen in 2-36% of cases. ,,, This resulted in an increase in false-negative and false-positive rates. ,,,, In these circumstances, open biopsy is recommended for definitive diagnosis. Tru-cut biopsies or CNBs provide sufficient tissue samples when compared to FNA. ,,,,,, Tru-cut or core needle biopsy (CNB) is less invasive when compared to open surgery. The volume of tissue removed and the degree of breast deformity are also much reduced in CNB. 
Although breast cancer assessment by either FNA or tru-cut biopsy has been considered the standard of care for more than a decade, it is still not a routine procedure in many developing countries.  In some of these developing countries the women are symptomatic at presentation and mostly in Breast cancer Stage II -III. ,,, For such women, the usual approach to sampling palpable lesions is either excisional or incisional biopsy, with or without intraoperative assessment by frozen section, all of which are no longer the acceptable standard of care of breast lesions.  When preoperative confirmation of cancer is facilitated by core biopsy, the numbers of surgeries are usually significantly decreased.  The total cost of breast cancer diagnosis and treatment is also decreased.  Another important concept in breast cancer care is the multidisciplinary team work as is the case with the Ibadan Multidisciplinary Breast Tumor Board in our hospital. The multidisciplinary approach aims at complying with international best practices in cancer care, providing the best available care, minimizing invasion to the patient while increasing the accuracy and quality of care. However despite cost-effectiveness and all the other advantages of this concept, it is still not yet widely accepted in some developing countries. ,,,
This study was carried out by the Ibadan Multidisciplinary Breast Tumor Board, a premier organ-specific tumour board in the Hospital. It is our initial experience on ultrasound-guided core biopsy of breast masses. FNA is frequently used for diagnosing image-detected breast lesions but there are some disadvantages which include: Insufficient sampling, inconclusive cytology result, false-negative cytology result, and inability to distinguish in situ from invasive carcinoma.  Open surgical biopsy, though the gold standard for diagnosis of image detected breast lesions, requires local or general anaesthesia, which usually necessitates an access wound that compromises cosmetic and future surgical options. A less invasive method of tissue sampling such as CNB is therefore beneficial. Even though this study reports our experience over four years, the study population was just forty due to local challenges of the mammography unit and limited funding for consumables. The age group of the women in this study is in agreement with the demography of previous local reports of women presenting with breast lesions. 
Ultrasound-guided biopsy has few limitations like localization of lesions and difficulties in obtaining adequate samples which could result in diagnostic errors.  These limitations were overcome by our multidisciplinary teamwork with close collaboration between the surgeon, radiologist, and pathologists as reported by other authors. ,,, All breast lesions were palpable, unlike studies by Joulae et al. where 40% were impalpable.  This contrast is probably due to the widely reported late presentation in Nigerian women a sequelae of the absence of a National Screening Programme and relatively low level of health awareness by our patients.  In such late presentations of palpable breast lesions, the tradition in our center over the decades has been to undertake a non-image guided tru-cut biopsy for diagnostic purpose. In many cases no imaging or FNA is performed as pre-operative assessment, thus falling short of the contemporary triple test (TT) approach to breast cancer evaluation.
The diagnostic TT of imaging, clinical breast examination (CBE), and CNB allow the surgeon to reduce the number of surgical biopsies for palpable breast lumps that prove to be benign, while at the same time effectively diagnosing cancer. In the classic TT strategy, the surgeon correlates the CBE, mammogram and FNA results to assess whether a palpable mass may be followed clinically instead of requiring an open biopsy. If all three are interpreted as benign (concordant-benign), the mass can be safely followed without excision. If all are malignant (concordant-malignant), the patient can proceed directly to definitive therapy without the need for intervening confirmatory open biopsy. If the three components are not in agreement (disconcordant), the mass should be histologically biopsied (CNB or surgical biopsy) for further evaluation. 
Errors from the pathologist in histologic diagnosis of a sample obtained by CNB or surgical biopsy of a breast lesion may occur due to a sampling technique that does not evaluate the entire volume of the biopsy specimen. Therefore, it is important that the histologic diagnosis be correlated with the clinical and imaging findings. The radiologist and/or the surgeon may perform this correlation. If the clinical and imaging findings are discordant with a benign histologic diagnosis, the pathologist should do further tissue sectioning because the initial sections may have missed the lesion. If they continue to be discordant, mammography should be repeated to see if the lesion was actually removed. Occasionally re-biopsy may be necessary. In essence, it is strongly recommended that the best diagnostic evaluation of breast problems occur when the primary care physician, radiologist, surgeon, and pathologist have an open and cooperative relationship.
Therefore hospitalization, surgery intraoperative frozen section, postoperative care, and long periods of absence from work are avoidable expenses that are erroneously paid to detect only a small number of cancers.  Tru-cut biopsy however performs the same evaluation for these masses with significant decrease in total expenses, especially in developing countries where late presentation and absence of a National Screening Programme are hallmarks of the management of the disease. Previous reports have documented unnecessary increase in the number of surgeries in patients managed with excision biopsy unlike tru-cut biopsies when a single surgery could suffice. ,
The majority (88%) of the suspicious breast lesions in BI-RADS Category 4 and 5 were found to be invasive ductal carcinoma. This contrasts with current trends in breast cancer care where majority of breast lesions diagnosed are carcinoma in situ. However, with increased advocacy and awareness campaigns by all stakeholders including the multidisciplinary team, it is believed that diagnosed tumors will soon be down staged.
The women with benign lesions were not offered any surgery; rather a follow-up study was recommended, an added advantage of CNB over excisional biopsy. The core specimens were also adequate for immunohistochemistry. Triple-negative tumors were found to be predominant in the cancers. This lends support to findings by previous reports in black women confirming the over representation of triple-negative breast cancer.  The triple-negative cancer common in these women is premenopausal which again reiterates the age range of breast cancer in women in the Nigerian setting. This preoperative determination of immune status of tumors is central in targeted therapy, which is now the global trend of breast cancer management.
Histological reports could sometimes be at discordance with clinical and radiological diagnosis consequently necessitating the surgeon to perform simple or guided biopsy as a diagnostic procedure this was not reported in our study.  Our study showed a false-positivity rate of less than 1% [Table 2] like that of Joulae et al. and there was no false-negative report.  These low rates of false-positivity and false-negativity may be due to the fact that all the masses in the study were palpable. Pain was the most common side effect in this series, and is expected to reduce as radiologists master the technique; however this pain subsided spontaneously in all the patients. Haematoma, a known complication of the procedure, was reported in only one of our patients and that procedure was immediately abandoned.  The high specificity and sensitivity of this study is a pointer to the accuracy of this relatively new approach to breast cancer management in Nigeria. This will in turn significantly increase the accuracy and quality of obtaining diagnostic tissue and ultimately contribute positively to the care in these patients. In addition there will be a notable decrease in patient invasion, diagnostic error, and total cost of management. ,,,,
| Conclusion|| |
This study shows that CNB/tru-cut biopsies can effectively be routinely used as a part of the World Health Organization (WHO) recommendation triple-test assessment for suspicious breast lesions in our center. Its reported benefits are elaborated in the impalpable masses when the targeted ultrasound guided biopsy increases accuracy of diagnosis with a significant decrease in the overall cost of management of the disease. It is recommended that it replaces the sole use of non-image guided surgical biopsies especially in a health resource-poor country like ours. The paper also emphasizes the value of multidisciplinary teamwork in the overall success of the planning, execution, and laboratory evaluation of specimens obtained from this unique technique.
| Acknowledgement|| |
The authors would like to acknowledge all the members of the various professional units of the Ibadan Multidisciplinary Breast Tumor Board. We are particularly indebted to the Global Health Initiative (GHI) chaired by Professor Olufunmilayo I Olopade for providing the accessories used for the CNB/tru-cut biopsies.
Source of funding
No financial support exists.
Conflicts of interest
There are no conflicts of interest.
| References|| |
Martin HE, Ellis EB. Biopsy by needle puncture and aspiration. Ann Surg 1930;92:169-81.
Fornage B, Peetrons P, Djelassi L Andry E, Faroux MJ, Pluot M, et al
. Ultrasound guided puncture of breast masses. J Belge Radiol 1987;70:287-98.
Masood S. Recent updates in breast fine needle aspiration biopsy. Breast J 1996;2:1-12.
Joulaee A, Kalantari M, Kadivar M, Joulaee S, Bahrani N, Mangual M, et al
. Trucut biopsy of breast lesions: The first step toward international standards in developing countries. Eur J Cancer 2012;5:648-54.
Patel JJ, Gartell PC, Smallwood JA, Herbert A, Royle G, Buchanan R, et al
. Fine needle aspiration cytology of breast masses: An evaluation of its accuracy and reasons for diagnostic failure. Ann R Coll Surg Engl 1987;69:156-9.
Pisano ED, Fajardo LL, Tsimikas J, Sneige N, Frable WJ, Gatsonis CA, et al
. Rate of insufficient samples for fine-needle aspiration for nonpalpable breast lesions in a multicenter clinical trial: The Radiologic Diagnostic Oncology Group 5 Study. The RDOG5 investigators. Cancer 1998;82:679-88.
Masood S. Core needle biopsy versus fine needle aspiration biopsy: Are there similar sampling and diagnostic issues? Clin Lab Med 2005;25:679-88, vi.
Parker SH. Needle selection. In: Parker SH, Jobe WE, editors. Percutaneous Breast Biopsy. New York: Raven Press; 1993. p. 7-14.
Mendelson EB, Tobin CE. Critical pathways in using breast US. Radiographics 1995;15:935-45.
Liberman L, Dershaw DD, Rosen PP, Giess CS, Cohen MA, Abramson AF, et al
. Stereotaxic core needle biopsy of breast carcinoma: Accuracy at predicting invasion. Radiology 1995;194:379-81.
Mainiero MB, Philpotts LE, Lee CH, Lange RC, Carter D, Tocino I. Stereotaxic core needle biopsy of breast microcalcifications: Correlation of target accuracy and diagnosis with lesion size. Radiology 1996;198:665-9.
Hung WK, Lam HS, Lau Y, Chan CM, Yip AW. Diagnostic accuracy of vacuum-assisted biopsy device for image-detected breast lesions. ANZ J Surg 2001;71:457-60.
Perry NM.; EUSOMA Working Party. Quality assurance in the diagnosis of breast disease. EUSOMA Working Party. Eur J Cancer 2001;37:159-72.
Montazeri A, Ebrahimi M, Mehrdad N, Ansari M, Sajadian A. Delayed presentation in breast cancer: A study in Iranian women. BMC Womens Health 2003;3:4.
Anderson BO, Jakesz R. Breast cancer issues in developing countries: An overview of the Breast Health Global Initiative. World J Surg 2008;32:2578-85.
Montazeri A, Vahdaninia M, Harirchi I, Harirchi AM, Sajadian A, Khaleghi F, et al
. Breast cancer in Iran: Need for greater women awareness of warning signs and effective screening methods. Asia Pac Fam Med 2008;7:6.
Harirchi I, Kolahdoozan S, Karbakhsh M, Chegini N, Mohseni SM, Montazeri A, et al
. Twenty years of breast cancer in Iran: Downstaging without a formal screening program. Ann Oncol 2011;22:93-7.
Ralleigh G, Michell M, Henderson S, Bose S. Does preoperative diagnosis reduce the number of operations required for treatment of screen-detected breast cancer? Breast Cancer Res 2000;2(Suppl 2):A30.
Blamey RW, Cataliotti L. EUSOMA accreditation of breast units. Eur J Cancer 2006;42:1331-7.
Winchester DP. The national accreditation program for breast centers: A multidisciplinary approach to improve the quality of care for patients with diseases of the breast. Breast J 2008;14:409-11.
American Cancer Society. Cancer Facts and Figures. Atlanta: American Cancer Society; 2014. p. 9-11.
Silverstein MJ. The Van Nuys Breast Center. The first free-standing multidisciplinary breast center. Surg Oncol Clin N Am 2003;9:159-75.
Gentry CL, Henry CA. Stereotactic percutaneous breast biopsy: A comparative analysis between surgeons and radiologist. Breast J 1999;5:101-4.
Irabor D, Okolo CA. An Audit of 149 consecutive breast biopsies in Ibadan, Nigeria. Pak J Med Sci 2008;24:257-62.
Vargas IH, Masood S. Implementation of a minimal invasive breast biopsy program in countries with limited resources. Breast J 2003;9(Suppl 2):S81-5.
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.
Vetto JT, Pommier R, Schmidt W, Wachtel M, DuBois P, Jones M, et al
. Use of the "triple test" for palpable breast lesions yields high diagnostic accuracy and cost savings. Am J Surg 1995;169:519-22.
Huo D, Ikpatt F, Khramtsov A, Dangou JM, Nanda R, Dignam J, et al
. Population differences in breast cancer: Survey in indigenous African women reveals over-representation of triple-negative breast cancer. J Clin Oncol 2009;27:4515-21.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
[Table 1], [Table 2]