|Year : 2018 | Volume
| Issue : 2 | Page : 79-86
Sonographic evaluation of axillary lymph nodes in women with newly diagnosed breast cancer at the university college hospital Ibadan, Nigeria
Atiku Hafiz1, Adenike Temitayo Adeniji-Sofoluwe2, Adeyinka Francis Ademola3, Millicent Olubunmi Obajimi2
1 Department of Radiology, University College Hospital, Ibadan, Nigeria
2 Department of Radiology, College of Medicine, University of Ibadan, University College Hospital, Ibadan, Nigeria
3 Department of Surgery, College of Medicine, University of Ibadan, University College Hospital, Ibadan, Nigeria
|Date of Web Publication||19-Jul-2018|
Adenike Temitayo Adeniji-Sofoluwe
Department of Radiology, College of Medicine, University of Ibadan/University College Hospital, Ibadan
Source of Support: None, Conflict of Interest: None
Background: Axillary lymph node (LN) status of patients with breast cancer is important in the surgical management. Sonographic evaluation of axillary LNs in newly diagnosed breast cancer is required to predict prognosis. Objective: The purpose of this study was to describe the morphologic features by sonographic evaluation of the cortices and sinuses as well as patterns of blood flow of axillary LNs and correlate same with the clinical staging in women with newly diagnosed breast cancer in a tertiary referral centre. Patients and Methods: This was a prospective and descriptive study of 106 newly diagnosed female breast cancer patients recruited from the surgical outpatient clinic of the University College Hospital, Ibadan, during a period of 9 months in 2015. All 106 patients had clinical evaluation, sociodemographic documentation and ultrasound scans of the breast and axillae performed. Results: The mean age of patients was 48.1 (±11.1) years with age range 20–82 years. Most patients have a negative family history of breast cancer as seen in 97 (91.4%) of them. Abnormal cortex-hilum area ratio was more frequent in the right (66.7%) than the left (41.2%) axillary LNs. Longitudinal-transverse ratio was abnormal in 93.5% and 86.3% of LNs in the right and left axillae, respectively. Slit-like hilum, eccentric cortical thickening, replaced node and rat-bite appearance, respectively, were found in 40.7%, 10.4%, 48.4% and 44.4% of LNs in the right axilla. The peripheral flow type was demonstrated in 46.8% and 48.1% of LNs in the right and left axillae, respectively. Conclusion: Ultrasonography is a good diagnostic tool that can be employed with reasonable accuracy in the initial assessment of axillary involvement in breast cancer. Although the assessment of tumour size and clinical staging leaves little doubt as to the stage of breast cancer disease, sonographic evaluation of the breast and the axilla painted a more ominous picture.
Keywords: Axillary lymph nodes, breast cancer, ultrasound
|How to cite this article:|
Hafiz A, Adeniji-Sofoluwe AT, Ademola AF, Obajimi MO. Sonographic evaluation of axillary lymph nodes in women with newly diagnosed breast cancer at the university college hospital Ibadan, Nigeria. Niger Postgrad Med J 2018;25:79-86
|How to cite this URL:|
Hafiz A, Adeniji-Sofoluwe AT, Ademola AF, Obajimi MO. Sonographic evaluation of axillary lymph nodes in women with newly diagnosed breast cancer at the university college hospital Ibadan, Nigeria. Niger Postgrad Med J [serial online] 2018 [cited 2019 Jul 20];25:79-86. Available from: http://www.npmj.org/text.asp?2018/25/2/79/237091
| Introduction|| |
Breast cancer is the most common cancer in women and the second most common cancer in the world. Approximately estimated 2 million new cancer cases were diagnosed in 2012., One million new cases are expected yearly in African countries by 2020 with estimated 500,000 cases expected in Nigeria alone.,, In Africa, breast cancer patients tend to present with histologically aggressive and more advanced disease with resultant poorer clinical outcomes compared with Caucasian patients. Breast cancer in Africans is often diagnosed at an average age of about 47 years while Caucasians are diagnosed after 65 years in Europe and America.,
A definitive histologic diagnosis is essential in suspected breast cancer cases. Imaging is part of preliminary methods utilised to stage breast cancer.,, Breast ultrasound is the most useful adjunctive breast imaging modality for lesion localisation and guided biopsies., Mammography remains the gold standard for breast cancer screening, recommended for all women ≥40 years regardless of risk assessment. Despite the benefit of mammography, there are limitations in dense tissues within very dense breasts. Identification and detection of metastasis in axillary lymph node (LN) is very important in patients with breast cancer to stage, choose appropriate treatment and determine prognosis.,,,,,
Sentinel LN biopsy (SLNB) is the diagnostic method of choice to determine the axillary LN status.,,, Ultrasound (US) is the primary imaging modality for evaluating axillary LNs.,,, The morphologic criteria, such as cortical thickening, hilar effacement, non-hilar cortical blood flow, compression of the hyperechoic medullary region and markedly hypoechoic cortex, are more important than size criteria in the identification of metastases.,,,,,,,, However, the accuracy of US for the evaluation of LN metastasis depends on the size of LNs., In cases with non-palpable small-sized LNs, the accuracy of US is reported to be limited, and the overall sensitivity of US ranges between 56% and 75% and specificity 70%–90%. Therefore, US alone is not sufficient to make a diagnosis of LN metastasis. If a suspicious LN is detected on US, ultrasound-guided intervention is recommended.,, The status of axillary LNs and other regional LNs is vital in the initial staging of breast cancer.,,,,,,, In the evaluation of LNs for metastases, eccentric and cortical morphologic changes are important, but the former has not been fully explored.,,,, The cortical thickness of a normal LN is 1–2 mm and >2.3 mm for an abnormal LN.,
The involvement of axillary LN in breast cancer plays a key role in staging, management and prognosis of the disease. Breast cancer with axillary LN metastases results in 4–5 times mortality rates in contrast to node-negative disease. There is also a positive relationship between positive LN status and the possibility of distant metastasis., Ultrasound is the most frequently utilised imaging modality for the investigation of the axilla because of the ease of its use, non-ionising properties and accessibility. Detection of morphological changes in axillary LNs as well as vascularity can be assessed before surgery. Identifying breast cancer patients with positive LNs preoperatively using ultrasound will allow patients to proceed directly to single-staged breast and axillary surgery without performing SLNB which is time-consuming and requires technical expertise which is not available in all centres and is not cost-effective.,,, There is, however, dearth of literature on breast cancer in Africa with regard to sonographic evaluation of axillary LN status in women with breast cancer, hence the need for this study. The purpose of this study was to bridge the gap in knowledge by providing data on the most common sonographic features (cortical morphology and pattern of blood flow) of axillary LNs seen in women with newly diagnosed breast cancer disease and to correlate clinical staging of axillary LNs in breast cancer with sonographic evaluation.
| Patients and Methods|| |
Ethical approval for this study was obtained from the University of Ibadan (UI)/University College Hospital (UCH) Ethics Committee at the Institute for Advanced Medical Research and Training of the College of Medicine, UI, Ibadan, Nigeria, with registration number NHREC/05/01/2008a. Ethical approval (protocol number- UI/EC/14/0315) was granted on 2nd April 2015. Written informed consent was obtained from all the participants.
This prospective descriptive study was conducted at the surgical oncology outpatient clinic and radiology department of the UCH, Ibadan, a tertiary referral centre in South West Nigeria. One hundred and six consenting newly diagnosed female patients with histology-proven (fine-needle aspiration cytology [FNAC] ± core-needle biopsy [CNB]) breast cancer were recruited during a 9-month period from April to December 2015. Women with previously diagnosed breast cancer who had chemotherapeutic or surgical intervention, history of rheumatoid arthritis, previous history of lymphoma and previous history of other cancers were excluded from the study. Eligible consenting patients had sociodemographic data, clinical history, clinical breast examination (CBE) findings, tumour stage (Manchester), FNAC and/or core-needle results obtained from their case notes and documented in the pro forma questionnaire. Breast and axillary ultrasound scans were performed in all patients.
Manchester breast cancer staging
This is a four-stage classification of breast cancer clinical assessment that was first adopted in 1940 at Christie Hospital in Manchester and is still widely used.
- Stage 1 is growth confined to the breast
- Stage 2 is growth confined to the breast, but mobile palpable nodes are present in the axilla
- Stage 3 is growth that extends beyond the breast parenchyma to involve the overlying skin or underlying muscle and axillary LNs that are still mobile
- Stage 4 is growth that extends beyond the breast parenchyma with fixation to the chest wall, fixed and matted axillary LNs with metastatic deposits to the supraclavicular LNs, opposite breasts and distant sites.
Technique of sonographic evaluation of the breast and axillary lymph nodes
The breast ultrasound scan procedure was explained to the patients and written informed consent was obtained. All patients were scanned in a private cubicle using the Logiq P5 (General Electric) ultrasound machine with 7.5–10 MHz linear array transducer. A nurse positioned patients on the couch, in the contralateral posterior oblique position, and a medium sized pillow was placed under the patient's shoulder, to prop up the breast and the ipsilateral axilla. The ipsilateral hand was placed behind the patient's head giving a clear access to the axilla. Both breasts were scanned in orthogonal planes after applying coupling gel to the scan area. The breast density and presence of any mass, its features, location and dimensions were documented. Both axillae were scanned, and the presence of nodes and features of the demonstrated nodes such as overall LN shape, assessment of the cortex and hilum, in abnormal LNs, the thickness of the cortex, the location outline and thickness of the hilum were all recorded. On Doppler interrogation, the presence and location of the blood vessels plus the presence of neovascularisation were documented. Final Breast Imaging Reporting and Data System (BIRADS) category of the breast was then assigned and documented.
The use of a high-frequency linear array transducer (7.5–10 MHz) permits a detailed sonographic analysis of the internal architecture of axillary LNs. There is a distinct differentiation of the central echogenic hilum which denotes multiple reflective interface of blood vessels, fat and central sinus, from the peripheral concentric hypoechoic cortex [Figure 1], which represents the marginal sinus, lymphoid follicles and paracortex., LN size and shape, cortical morphology, presence or absence of an echogenic hilum, nodal border, echogenicity, calcification/cystic-necrotic changes and vascular configurations are some sonographic features to characterise LN as benign or malignant. A LN with uniformly thickened cortex is usually reactive while eccentric cortical thickening and convex dents of the mediastinum (rat bites) support metastatic disease. Other features of metastatic LNs are slit-like pattern of the hilum, eccentric compression and displacement of the hilum to the edge of the node, complete mediastinal obliteration, rounding of the LN, perinodal invasion with irregularity and loss of definite margins.,,,,
|Figure 1: Ultrasound scan of the axilla. Longitudinal view of a normal/benign oval-shaped lymph node with smooth cortical outline central echogenic hilum (blue cursors)|
Click here to view
Doppler sonography of axillary lymph node
Doppler ultrasound (US) is a non-invasive form of angiography utilised to assess neovascularisation and angiogenesis which are characteristic features of malignant lesions including breast cancer. The arterial supply of a normal LN comes in through the hilum usually in a single artery. Inflammation causes vasodilatation and increased flow but does not result in angiogenesis and neovascularisation, which is stimulated in neoplasms. Thus, neoplastic LNs, unlike inflamed nodes, have multiple feeding arteries. Most LNs >5 mm in size will demonstrate flow in 90% of cases; however, smaller nodes with small vessels and normal and reactive LNs may not show demonstrable flow.,, In metastatic axillary LNs, high systolic and diastolic flow with abnormal vascular shunting results in an abnormal flow pattern and angio-architecture due to angiogenesis factors. The generated data were analysed and frequency tables generated using the Statistical Package for the Social Sciences (SPSS) version 20.0 (IBM SPSS, Chicago, IL, USA, 2016). P value is set at 0.05 with 95% confidence interval. Other variables were presented as pie and bar charts.
| Results|| |
One hundred and six female patients were recruited into the study. The mean age of the patients was 48.1 (±11.1) years with age range between 20 and 82 years. Most patients, i.e. 37/106 (34.9%) were in the age group of 40–49 years, while the majority of patients, i.e. 91/106 (85.8%) were married. [Table 1] summarises the sociodemographic characteristics of patients while [Table 2] presents their general examination and clinical history. The mean age at menarche was 15.3 years (standard deviation [SD] = 1.9) while the mean age at menopause was 50.7 years (SD = 5.6). A negative family history of breast cancer was elicited in 97 patients (91.4%). About half of the patients had previous breast examinations (57.5%) with self-breast and CBEs frequently mentioned by 88.5% and 44.3% of the women, respectively. All but one (98.4%) patient with a previous history of breast examination detected breast lumps.
The most frequent location of breast lumps found at CBE was in the upper outer quadrant of both breasts in 92 patients. Fifty-two (56.5%) masses were in the right breast and 39 (42.4%) in the left breast with bilateral lumps in only one patient. The lower outer quadrant was the next most frequent site for breast masses in 77 patients. Seventy-two retroareolar masses were detected, with 40 (55.6%) located in the right breast, 31 (43.1%) in the left breast and 1 (1.4%) in both breasts. There were more intramammary masses than axillary lesions. LNs were palpable in the majority of patients, i.e. 86/106 (81.1%) with more LNs in the right axilla 44/106 (51.2%) than in the left axilla 34/106 (39.5%) while 8/106 (9.3%) bilateral axillary LNs were palpated [Table 3].
The findings at breast and axillary ultrasound scan are depicted in [Figure 2], [Figure 3], [Figure 4], [Figure 5]. The heterogeneously dense breast was the predominant breast pattern (62.3%), subsequently homogeneous fatty (31.1%) and homogeneous dense (2.8%) breast. A global breast mass was seen in less than half (44/106, 41.5%) of the patients. Amongst 92 cases with palpable nodes in the axilla, 7 (10.9%) had single nodes while 55 (85.9%) had multiple nodes in the right axilla with slightly more than half of the nodes in the right axilla with irregular (51.6%), oval (46.0%) and round (27.4%) shapes. In patients with nodes in the left axilla, 46 (80.7%) had multiple nodes while 5 (8.8%) had single nodes. Majority of the nodes in the left axilla were oval (52.7%), irregular (38.9%) and round (24.1%). LN measurements in patients were recorded. The mean cortex/hilum area ratio in the right axilla was 2.3 (SD = 0.8) and that of the left was 2.7 (SD = 2.4). The longitudinal/transverse area ratio in the right axilla was 1.3 (SD = 0.6) and that of the left axilla was 1.5 (SD = 0.4). Abnormal cortex/hilum area ratio was seen more frequently in right axillary LNs in 66.7% than in the left axillary LNs in 41.2%. Furthermore, an abnormal longitudinal/transverse ratio was seen in 93.5% and 86.3% of LNs in the right and left axillae, respectively. The peripheral flow type was demonstrated predominantly in 46.8% and 48.1% of LNs in the right and left axillae, respectively. Other vascular flow types documented were central flow (15.1% and 22.2%), clumped flow (19.4% and 20.4%) and normal flow (17.7% and 14.8%) in the right and left axillae, respectively [Figure 4].
|Figure 4: Axillary ultrasound scan with Doppler interrogation in longitudinal view showing (a) eccentric hypoechoic thickening with peripherally displaced hyperechoic hilum (white star) with transcapsular neovascularisation (orange arrow), (b) extensive replacement of lymph node cortex by metastatic tumour eccentrically compressing the hilum to the edge of the node (small white arrows) and neovascularisation (orange arrows) and (c) an enlarged lymph node with a completely obliterated hilum, clumped centrally located vessels (small white arrows) and transcapsular vessels (orange arrows)|
Click here to view
|Figure 5: Axillary lymph node ultrasound scan with Doppler interrogation showing (a) transverse view with a severely infiltrated axillary lymph node cortex (white stars) with an eccentric compressed hilum-characteristic slit-like hilar appearance (white arrow), (b) an abnormal node with multiple cortical lobulations (transparent white arrows) and convex inwards non-uniform and eccentric indentations ‘rat bites’ of the hilum (white arrowheads) and (c) an axillary lymph node with loss of outer thin echogenic capsule (white dashes arrows), in antiparallel orientation (white arrows) with angular margins|
Click here to view
Manchester stages [Table 4] IIA and IIIB were the most common (18.1%) clinical stages of breast cancer made in all 106 women. This was followed by Stages IIB and IIIC (17.1%), Stage IIIA (14.3%), Stage IV (10.5%), Stage IB (3.8%) and Stage IIC (1.0%). The breast lump size in patients also varied with about one-third classified as T1a (35.9%) and T1c (35.0%). Others were T1b (28.0%) and T1 mi (1%). The predominant BIRADS assessment categories reported on ultrasound were Category 5 (77.4% – highly suggestive of malignancy), Category 4 (15.1% – suspicious findings) and Category 6 (0.9% – biopsy-proven cancer).
|Table 4: Manchester breast cancer stage amongst 106 breast cancer patients|
Click here to view
| Discussion|| |
LN status is very important in the initial staging of breast cancer.,, Several studies now show the importance of ultrasound combined with fine-needle aspiration in the pre-operative assessment of the axilla for the presence of metastasis as mammography and physical examination have limited value in this regard.,, Therefore, ultrasound evaluation should be incorporated into the initial evaluation of suspected breast cancer patients, especially as it is a cheap, accessible and a relatively accurate means of staging. Ultrasound shows excellent anatomical details of LNs that are reproducible. Major sonographic criteria for metastatic LNs have focussed on node shape and echogenicity, but focal cortical morphologic changes may be more important because of a centrifugal pattern of metastatic cell deposits.,,,
Axillary node status is a well-known key prognostic indicator and management guide for breast cancer.,,,,,,,,,,,,,,,,, Consequently, there is a growing need to stage breast cancer precisely, especially with ultrasound imaging. Axillary dissection is the conventional method of evaluation of axillary LNs histologically and therapeutically to decrease the risk of axillary recurrence.,,,,,, Complete axillary dissection increases morbidity and gives no additional benefit in node-negative breast cancer.,,
Clinical breast cancer staging in our study showed 18.1% of the patients presented at Stages IIA and IIIB while Stage IIIA constituted 14.3% and those in Stage IV constituted 10.5%. Tumour size assessment amongst the patients showed tumour Stages T1a (35.9%) and T1c (35.0%) predominance. Final BIRADS Category 5 constituted 77.5% of the patients; this shows a high correlation between ultrasonography and clinical findings when breast cancer is suspected. These findings are consistent with the pattern of late presentation of African breast cancer seen in other studies.,,,,,,,, Although the assessment of tumour size and clinical staging leaves little doubt as to the stage of breast cancer presentation in the cohort, sonographic evaluation of the breast and the axilla painted a more ominous picture. In this regard, ultrasound is a far more useful tool than clinical examination alone. Several researchers have documented similar findings.,,,,,, Oruwari et al. in 2002 showed that ultrasound was superior to clinical assessment to determine axillary LN status in 26 breast cancer patients with sensitivity and specificity of 91% and 92%, respectively. In the same vein, Sapino et al.in their study of 298 patients in Italy demonstrated that ultrasound showed high specificity, was cheap and readily available and hence endorsed axillary evaluation by ultrasound before surgical intervention in breast cancer patients.
Several grey-scale sonographic and Doppler characteristic findings have been documented in the literature to aid in the recognition of abnormal axillary nodes.,,,,,,,,, The emphasis is on the cortical features in the morphologic assessment of LNs.,,, Metastasis initially involves the subcapsular and cortical sinuses in a centrifugal manner through the afferent lymphatic channels. Metastatic invasion of subcapsular and cortical sinuses is eccentric giving the characteristic eccentrically enlarged cortex. Amongst the study population, the proportion of LNs with eccentrically enlarged cortex was more in the right axilla [Figure 3]. Severe concentric or nearly concentric compression of the hilum by thickened cortex may make the residual hyperechoic hilar tissue appear slit-like. In this study, we found 40.7% of patients with the slit-like hilum in the left axilla [Figure 5]. Severe eccentric cortical thickening completely displaces the hilum of a LN to one edge which was demonstrated in the right axilla in 10.4% and left axilla in 15.9% of patients. It is a specific finding for metastatic disease which rarely occurs in inflammatory conditions. In the most severely abnormal LN, the hilar echoes can become completely obliterated and non-identifiable because of complete compression or complete displacement outside of the node. Such severe involvement is more typical of metastatic disease than inflammation but can occur in necrotising lymphadenitis. In this study, 31 (48.4%) and 22 (40.7%) patients demonstrated this LN appearance on the right and left sides, respectively.
Conversely, early metastatic deposits lodge in the deep cortical sinuses rather than the subcapsular sinusoids resulting in focal thickening of the inner cortex of the LN that manifests as convex inwards indentation of the hyperechoic LN mediastinum by hypoechoic cortex giving the characteristic rat-bite appearance [Figure 5]. Our study population showed 28 (44.4%) and 18 (34.0%) patients with this feature in their right and left axillae, respectively. In 85% of breast cancer cases, the primary tumour shares histologic type with the metastatic LNs., Various Doppler ultrasound criteria such as branching pattern, flow resistance and spectral analysis have been used by several studies to differentiate benign from malignant breast lesions., These studies found more commonly in metastatic LNs, the central pattern. Other parameters utilised such as resistivity, pulsatility indices and peak systolic velocity, did not discriminate malignant from benign axillary LNs, as previously demonstrated in cervical LNs. Doppler ultrasound is useful when used in conjunction with other diagnostic features and not alone.,,
Blood flow to normal, reactive or inflamed LN passes into the node through the capsule. Therefore, neoplastic nodes, unlike inflamed nodes, frequently have several feeding vessels. Transcapsular feeding vessels are particularly specific for metastatic disease. The predominant Doppler flow type in this study was peripheral reported in 46.8% and 48.1% of LNs in the right and left axillae, respectively. Kwak et al. evaluated 353 solid breast lesions with power Doppler to evaluate LN metastasis and reported considerably more penetrating vessels in malignant lesions.
Many authors have developed classifications based on images of cortical thickness of axillary nodes found at ultrasound to suggest metastases. Cho et al. categorised images into five grades while Bedi et al. classified images into six types., LNs in Types 5 and 6 were considered suspicious. The literature sets a cut-off at 2.3–3 mm for cortical thickness in metastatic disease.,,,,, Some authors prefer the use of a cortex/hilum ratio, rather than an absolute value for the cortex. Therefore, cortical thickening is inferred when the maximum cortex thickness is ≥ the thickness of the fatty hilum.,, Song et al. in 2007 found a significantly higher sensitivity of cortex-hilum area ratio of 94.1% compared to longitudinal-transverse axis ratio of 82.3% and blood flow pattern in 29.4% in an attempt to diagnose metastatic axillary LNs by ultrasound in breast cancer patients. We found an abnormal cortex-hilum area ratio more frequently in the right axillary LNs in 66.7% than in the left axillary LNs in 41.2%. Furthermore, an abnormal longitudinal-transverse ratio was seen in 93.5% and 86.3% of LNs in the right and left axillae, respectively.
| Conclusion|| |
Ultrasonography is an important tool in the pre-operative evaluation of axillary LN status in breast cancer patients in Sub-Saharan Africa and resource-poor settings. The utilisation of this method allows for the identification of the axillary disease extent and assists in percutaneous biopsy. Changes such as cortical thickening and hilum absence are predictors of metastatic disease, and cytological or histological analysis is indicated in cases where such changes are present. From the findings of this study, majority of the patients presented with locally advanced disease that will benefit from ultrasonography combined with CNB and axillary clearance surgery. All the documented types of cortical axillary LN appearances in axillary LN metastasis were demonstrated with predominant final BIRADS Category 5 lesions in more than three-quarters of the patients, which further reaffirm the late presentation of breast cancer in Nigeria.
There is a need to routinely incorporate imaging of the breast and axilla in the evaluation of breast cancer patients for more accurate staging. This study has shown that imaging with ultrasound is superior to clinical evaluation of the breast cancers, therefore more useful for prognostic purposes. Multidisciplinary breast tumour boards should be encouraged to facilitate and harmonise clinical and imaging findings to improve patient management protocols and consequently patient outcomes.
We acknowledge the roles played by Prof. Ogundiran and are grateful to Mrs. Chibuzor and Mrs. Famooto of the surgical oncology unit who helped with recruitment of patients and all the Nursing staff, especially Matron Ogungbade.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, et al.
Cancer statistics, 2008. CA Cancer J Clin 2008;58:71-96.
DeSantis CE, Siegel RL, Sauer AG, Miller KD, Fedewa SA, Alcaraz KI, et al.
Cancer statistics for African Americans, 2016: Progress and opportunities in reducing racial disparities. CA Cancer J Clin 2016;66:290-308.
World Health Organization. Breast Cancer Estimated Incidence, Mortality and Prevalence Worldwide. GLOBOCAN 2012. Lyon France: IARC; 2012.
Opoku SY, Benwell M, Yarney J. Knowledge, attitudes, beliefs, behaviour and breast cancer screening practices in Ghana, West Africa. Pan Afr Med J 2012;11:28.
Adebamowo CA, Ogundiran TO, Adenipekun AA, Oyesegun RA, Campbell OB, Akang EE, et al.
Waist-hip ratio and breast cancer risk in urbanized Nigerian women. Breast Cancer Res 2003;5:R18-24.
Adebamowo CA, Adekunle OO. Case-controlled study of the epidemiological risk factors for breast cancer in Nigeria. Br J Surg 1999;86:665-8.
Berg WA, Blume JD, Cormack JB, Mendelson EB, Lehrer D, Böhm-Vélez M, et al.
Combined screening with ultrasound and mammography vs. mammography alone in women at elevated risk of breast cancer. JAMA 2008;299:2151-63.
Alvarez S, Añorbe E, Alcorta P, López F, Alonso I, Cortés J. Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: A systematic review. AJR Am J Roentgenol 2006;186:1342-8.
Jain SA, Agarwal L, Goyal A, Kumar R, Shravan, Ameta A, et al
. Study on efficacy of preoperative ultrasonography for axillary lymph node involvement in breast carcinoma. IOSR J Dent Med Sci 2014;13:1-5.
Mainiero MB, Cinelli CM, Koelliker SL, Graves TA, Chung MA. Axillary ultrasound and fine-needle aspiration in the preoperative evaluation of the breast cancer patient: An algorithm based on tumor size and lymph node appearance. AJR Am J Roentgenol 2010;195:1261-7.
Sickles EA, Filly RA, Callen PW. Breast cancer detection with sonography and mammography: Comparison using state-of-the-art equipment. AJR Am J Roentgenol 1983;140:843-5.
Brenin DR, Morrow M, Moughan J, Owen JB, Wilson JF, Winchester DP. Management of axillary lymph nodes in breast cancer: A national patterns of care study of 17,151 patients. Ann Surg 1999;230:686-91.
Cox CE, Pendas S, Cox JM, Joseph E, Shons AR, Yeatman T, et al.
Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg 1998;227:645-51.
Dogo D, Pindiga PU, Yawe T. Pattern of breast lesions in North Eastern Nigeria. Trop J Med Res 2000;3:14-7.
Zhao H, Zou L, Geng X, Zheng S. Limitations of mammography in the diagnosis of breast diseases compared with ultrasonography: A single-center retrospective analysis of 274 cases. Eur J Med Res 2015;20:49.
Torabi M, Aquino SL, Harisinghani MG. Current concepts in lymph node imaging. J Nucl Med 2004;45:1509-18.
Weir L, Speers C, D'yachkova Y, Olivotto IA. Prognostic significance of the number of axillary lymph nodes removed in patients with node-negative breast cancer. J Clin Oncol 2002;20:1793-9.
Cianfrocca M, Goldstein LJ. Prognostic and predictive factors in early-stage breast cancer. Oncologist 2004;9:606-16.
Krag D, Weaver D, Ashikaga T, Moffat F, Klimberg VS, Shriver C, et al.
The sentinel node in breast cancer – a multicenter validation study. N
Engl J Med 1998;339:941-6.
Cho N, Moon WK, Han W, Park IA, Cho J, Noh DY. Preoperative sonographic classification of axillary lymph nodes in patients with breast cancer: Node-to-node correlation with surgical histology and sentinel node biopsy results. AJR Am J Roentgenol 2009;193:1731-7.
Bonnema J, van Geel AN, van Ooijen B, Mali SP, Tjiam SL, Henzen-Logmans SC, et al.
Ultrasound-guided aspiration biopsy for detection of nonpalpable axillary node metastases in breast cancer patients: New diagnostic method. World J Surg 1997;21:270-4.
Moon HJ, Kim EK. Characteristics of breast cancer detected by supplementary screening ultrasonography. Ultrasonography 2015;34:153-6.
Song SE, Seo BK, Lee SH, Yie A, Lee KY, Cho KR, et al.
Classification of metastatic versus non-metastatic axillary nodes in breast cancer patients: Value of cortex-hilum area ratio with ultrasound. J Breast Cancer 2012;15:65-70.
Bedi DG, Krishnamurthy R, Krishnamurthy S, Edeiken BS, Le-Petross H, Fornage BD, et al.
Cortical morphologic features of axillary lymph nodes as a predictor of metastasis in breast cancer:In vitro
sonographic study. AJR Am J Roentgenol 2008;191:646-52.
Abe H, Schmidt RA, Kulkarni K, Sennett CA, Mueller JS, Newstead GM, et al.
Axillary lymph nodes suspicious for breast cancer metastasis: Sampling with US-guided 14-gauge core-needle biopsy – Clinical experience in 100 patients. Radiology 2009;250:41-9.
Stachs A, Göde K, Hartmann S, Stengel B, Nierling U, Dieterich M, et al.
Accuracy of axillary ultrasound in preoperative nodal staging of breast cancer – Size of metastases as limiting factor. Springerplus 2013;2:350.
Podkrajsek M, Music MM, Kadivec M, Zgajnar J, Besic N, Pogacnik A, et al.
Role of ultrasound in the preoperative staging of patients with breast cancer. Eur Radiol 2005;15:1044-50.
Mobbs LM, Jannicky EA, Weaver DL, Harvey SC. The accuracy of sonography in detecting abnormal axillary lymph nodes when breast cancer is present. JDMS2005;21:297-303.
Kwak JY, Kim EK, Kim MJ, Choi SH, Son E, Oh KK. Power Doppler sonography: Evaluation of solid breast lesions and correlation with lymph node metastasis. Clin Imaging 2008;32:167-71.
Rahbar H, Partridge SC, Javid SH, Lehman CD. Imaging axillary lymph nodes in patients with newly diagnosed breast cancer. Curr Probl Diagn Radiol 2012;41:149-58.
Stavros AT, Thickman D, Rapp CL, Dennis MA, Parker SH, Sisney GA, et al.
Solid breast nodules: Use of sonography to distinguish between benign and malignant lesions. Radiology 1995;196:123-34.
Stavros T. Breast Ultrasound. 1st
ed. Philadelphia Pennsylvania USA: Lippincott, Williams and Wilkins; 2013. p. 834-41.
Lee B, Lim AK, Krell J, Satchithananda K, Coombes RC, Lewis JS, et al.
The efficacy of axillary ultrasound in the detection of nodal metastasis in breast cancer. AJR Am J Roentgenol 2013;200:W314-20.
Odigie VI, Yusufu LM, Rafindadi A, da Rocha-Afodu JT. Breast cancer in Zaria. Nig J Surg 2003;9:46-50.
Thomas JO. Cancer registration and diagnosis in Ibadan. Arch Ibadan Med 2000;1:5-6.
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.
Akinola R, Wright K, Osunfidiya O, Orogbemi O, Akinola O. Mammography and mammographic screening: Are female patients at a teaching hospital in Lagos, Nigeria, aware of these procedures? Diagn Interv Radiol 2011;17:125-9.
Oruwari JU, Chung MA, Koelliker S, Steinhoff MM, Cady B. Axillary staging using ultrasound-guided fine needle aspiration biopsy in locally advanced breast cancer. Am J Surg 2002;184:307-9.
Sapino A, Cassoni P, Zanon E, Fraire F, Croce S, Coluccia C, et al.
Ultrasonographically-guided fine-needle aspiration of axillary lymph nodes: Role in breast cancer management. Br J Cancer 2003;88:702-6.
Oz A, Demirkazik FB, Akpinar MG, Soygur I, Baykal A, Onder SC, et al.
Efficiency of ultrasound and ultrasound-guided fine needle aspiration cytology in preoperative assessment of axillary lymph node metastases in breast cancer. J Breast Cancer 2012;15:211-7.
Shetty MK, Carpenter WS. Sonographic evaluation of isolated abnormal axillary lymph nodes identified on mammograms. J Ultrasound Med 2004;23:63-71.
Krishnamurthy S, Sneige N, Bedi DG, Edieken BS, Fornage BD, Kuerer HM, et al.
Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma. Cancer 2002;95:982-8.
Kish L. Survey Sampling. New York: John Wiley and Sons; 1965. p. 50-9.
Deurloo EE, Tanis PJ, Gilhuijs KG, Muller SH, Kröger R, Peterse JL, et al.
Reduction in the number of sentinel lymph node procedures by preoperative ultrasonography of the axilla in breast cancer. Eur J Cancer 2003;39:1068-73.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3], [Table 4]