|Year : 2014 | Volume
| Issue : 4 | Page : 839-845
Grading systems in the cytological diagnosis of breast cancer: A review
Cherry Bansal1, Mukta Pujani2, Kiran Lata Sharma3, AN Srivastava4, US Singh1
1 Department of Pathology, King George Medical University, Lucknow, Uttar Pradesh, India
2 Department of Pathology, Hamdard Institute of Medical Sciences and Research, New Delhi, India
3 Department of Surgical Oncology, King George Medical University, Lucknow, Uttar Pradesh, India
4 Department of Pathology, Era's Medical College and Hospital, Lucknow, Uttar Pradesh, India
|Date of Web Publication||9-Jan-2015|
Associate Professor, Department of Pathology, Hamdard Institute of Medical Sciences and Research, New Delhi - 110 062
Source of Support: None, Conflict of Interest: None
In developing countries, diagnosis of breast carcinoma is still made on fine-needle aspiration cytology (FNAC). For the resource-poor settings, FNAC is cheaper, less invasive and can sample different areas of the lesion compared with core needle biopsy. The role of breast FNA is usually limited to just categorize the lesion as benign or malignant. Prognostic information from cytomorphology, conveyed to the clinician depends upon the cytopathologist's way of formatting the report. PubMed-based literature search collated the information from articles describing the architectural and cytological features studied on breast aspiration smears. This review focuses on cytomorphological features and the different grading systems with their strengths, short-comings, and practical applicability. Eight worldwide articles proposing new methods of grading the cytological smears from breast cancers were published between 1980 and 2006. All the grading methods were developed for the most common type of breast cancer, that is, infiltrating duct carcinoma (not otherwise specified) type, and most of the workers used Papanicolaou-stained smears for the purpose of grading. Moreover, if interpreted carefully FNAC smears can convey information on most of the histological features. Hence, in developing countries, the focus should be on extracting the maximum information from cytological smears, so that a more precise "surgical pathology" type diagnosis can be given, instead of merely reporting as benign or malignant. Among all the discussed grading systems, we suggest grading system by Howell would be most appropriate and closest to the accepted histologic grading system as it applies Scarff-Bloom-Richardson histological grading system with modifications on FNA smears. We recommend it to be followed by all cytopathologists, in order to bring uniformity in the reporting of breast FNAs for grading the malignant lesions.
Keywords: Breast, carcinoma, cytological grading, fine-needle aspiration
|How to cite this article:|
Bansal C, Pujani M, Sharma KL, Srivastava A N, Singh U S. Grading systems in the cytological diagnosis of breast cancer: A review. J Can Res Ther 2014;10:839-45
|How to cite this URL:|
Bansal C, Pujani M, Sharma KL, Srivastava A N, Singh U S. Grading systems in the cytological diagnosis of breast cancer: A review. J Can Res Ther [serial online] 2014 [cited 2020 Jun 4];10:839-45. Available from: http://www.cancerjournal.net/text.asp?2014/10/4/839/140979
| > Introduction|| |
Breast carcinoma is the most common malignant tumor and the leading cause of cancer deaths in women with more than 1,000,000 cases occurring worldwide annually.  Accurate diagnosis of breast cancer is made in 99% of cases by the combination of clinical examination, mammography and simple, noninvasive, cost-effective outpatient department procedure, fine-needle aspiration cytology (FNAC). Technique of FNAC has wide applicability and utility for the tumors which are easily palpable on external examination. , In developed world, the practice and usefulness of breast FNA have been overshadowed by core needle biopsy. On the contrary, in developing countries like India, even today, the core needle biopsy is still not practiced routinely at most of the medical centers. The treatment of breast carcinoma cases is begun with the first hand diagnosis made on FNAC. Moreover, for resource-poor countries, FNA in comparison to core needle biopsy, is cheaper, less invasive, can sample different areas of the lesion in the same sitting at no added expenses and usually fetch good results the same day. , The acceptance of FNA report reliability both by surgeons and pathologists allows for radical surgery on the basis of an FNA diagnosis. Regrettably, instead of signing a more precise "surgical pathology" type diagnosis on FNA, its widest application is limited to just categorizing the breast lesion as benign or malignant. The prognostic markers important for deciding the treatment modality should be conveyed to the surgeon, as recognition of the aggressiveness of the disease is central to the effective medical management of breast cancer and avoid the needless morbidity. ,, This review discusses the various grading systems proposed by different authors over several years for breast carcinoma cytology.
| > Need to Mention Cytoloical Grading in Cytology Report?|| |
Cytopathologist's way of formatting the report determines whether accurate and complete information based on cytomorphology is conveyed to the clinician or not. In preference to the usual descriptive and subjective method of reporting the FNA smears, cytological grading should be included in the report.
Cytological grading mentioned in a cytology report, in actual fact, adds to objectivity, reproducibility, and authenticity of the particular report. The National Cancer Institute, Bethesda sponsored a conference on the "Uniform approach to report breast fine-needle aspiration biopsy." They also recommended that tumor grading on FNA material should be incorporated in cytology reports for prognostication. Furthermore, importance was laid on the cytological grading system which would correspond closely to the grading system used in the histological material, but the most reliable cytological grading method is yet to be determined. ,
The different grading systems used for breast cancer cytology are being compared. The study focuses on cytomorphological features and the scoring criteria considered by various authors for reporting breast carcinoma. The different grading methods have been discussed for their strengths, short-comings, and practical applicability.
Articles related to the different methods developed for breast carcinoma cytological grading were retrieved from the PubMed literature search. Present study includes the information collated from each article regarding the architectural and cytological features studied on breast aspiration smears, the method, and criteria for objective scoring. Grading criteria and cytomorphological features considered by various authors are tabulated and discussed for their utility and shortcomings.
| > Cytological grading systems for breast cancer|| |
Articles proposing new methods of grading breast FNA smears were published between 1980 and 2006. During this period, a total of 8 research papers from worldwide institutions was published introducing different new aspects of categorizing and scoring the breast FNA smears. Elaborated cytological criteria considered and scoring systems proposed by different investigators are tabulated [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7] and [Table 8]. All the grading methods were developed for the most common type of breast cancer, that is, infiltrating duct carcinoma (not otherwise specified) type. Majority of the researchers utilized Papanicolaou-stained smears for the purpose of grading. Number of cases ranged from 20 to 281 in these studies while Grade 2 carcinoma comprised majority of cases among the study groups. Nuclear features were invariably included in scoring scheme by all the researchers [Table 9]. Different grading methods are:
|Table 2: Fisher's simplification of Black's nuclear grading scheme (1980) |
Click here to view
|Table 4: Robinson's criteria (1994) for cytological grading of breast carcinoma |
Click here to view
|Table 7: Khan et al. proposed evaluation of cytomorphological characteristics |
Click here to view
|Table 9: Comparative table of cytomorphological studies by different authors |
Click here to view
Mouriquand's method of cytoprognostic classification (1980) was applied to both topographic and cytologic criteria and took into account the cellular characteristics, nuclear features, nucleoli, and number of mitoses , [Table 1].
Black's nuclear grading scheme comprises four grades, with Grade 1 equal to anaplasia and Grade 4; the best-differentiated grade.  This initial grading system was confusing, and Fisher simplified it, so as to match the big numeral grade with a higher degree of anaplasia. Fisher's simplification uses three grades, with Grade 1 representing the highest level of differentiation and Grade 3 equivalent to anaplasia  [Table 2].
Ten years later, Hunt et al.  in 1990 also studied the nuclear features as did by Fisher et al.,  but in addition, they proposed a scoring scheme for the nuclear features. Final grade was categorized into two groups, that is, low and high. Discriminant analysis showed that cytological grading into high and low; based on nuclear diameter, nuclear pleomorphism, and the presence of nucleoli had a close correlation with histological grade [Table 3].
In 1994, Robinson et al. introduced a grading system on Papanicolaou-stained cytosmears with a wider range of features including architectural arrangement, cellular details as well as nuclear characteristics [Table 4]. 
Howell et al.  in 1994 evaluated the application of the Scarff-Bloom-Richardson (SBR) histological tumor grading  to breast FNA aspirates. All the three features of SBR grading method, that is, tubule formation, nuclear pleomorphism, and mitoses were taken into consideration [Table 8].
Yu et al. in 1998 evaluated tumor cells (dys) cohesion as a prognostic factor in breast aspirates and assigned a "dyscohesion score" (DS).  The bases were the relative proportion of intact tumor cells and loosely cohesive tissue fragments in the aspirate smears. In addition to dyscohesion, they calculated nuclear grade by method used by Dabbs and Silverman , [Table 5].
Taniguchi et al. established a semi-quantitative scoring system composed of seven parameters with introduction of necrosis as a feature to be assessed on cytosmears.  Each of the seven cytologic features was assessed in accordance with 1-3 or 0-1 points. The scores were summed to arrive at a total cumulative score for a given case [Table 6].
Khan et al.  proposed an elaborated grading system which included cytological features not evaluated in the previous studies like lymphocytic response. The final tumor grade was assigned by adding the different scores obtained [Table 7].
Fan et al.  proposed a new grading system, combining nuclear grade (score 1-3 as per used by Fisher's modification of Black's nuclear grading scheme), cellular dyscohesion (score 1-3 as per used by Yu et al.  ), and bare atypical nuclei to arrive at a final cytoprognostic score. Bare atypical nuclei were scored by the absence (score 0) or presence (score 1) of large (>3 × red blood cell), irregular, coarse stripped nuclei in the background. Final cytoprognostic score was assigned as low if ≤ 3 and high if 4-7. A low cytoprognostic score predicted a low to intermediate grade carcinoma and a high score predicted an intermediate to high-grade carcinoma.
| > Histological grading for breast carcinoma|| |
Histological grading of breast carcinoma was first suggested in 1957 by Bloom and Richardson.  Initially, it was not a constant part of breast carcinoma histological evaluation due to the perception that the grading was difficult to perform and not reproducible. But, research results showed that the most important histomorphological prognostic factors for breast carcinoma patients were histologic type and nuclear grade. These are independent prognostic indicators that can predict overall and metastasis-free survival for local and regionalized breast carcinoma. Today, the value of breast carcinoma histological grading is well-established and assigning the tumor grade has prognostic implication which helps in guiding appropriate therapy. ,,
Breast carcinoma grading in isolation has prognostic value and has been recommended to form part of all surgical pathology reports. Elston's modified Bloom and Richardson (MRB) method to grade breast carcinoma scores tubule formation, cellular pleomorphism, and mitotic rate. Score varies from 3 to 9 and is summed up to assign one of the three histological grades [Table 8]. , National Institutes of Health Consensus conferences concluded that the key prognostic pathological factors for patients with breast carcinoma were tumor size, lymph node status, nuclear grade, histologic type, proliferative index, and hormonal status, and all these parameters should be included in the surgical pathology report of resected specimens. 
Nottingham prognostic index for breast carcinoma combines important prognostic factors such as MRB grade, lymph node metastasis, and tumor diameter. For neoadjuvant therapy, it can be utilized by estimating tumor diameter radiologically, tumor grade by cytology, and lymph node status by staging lymphadenectomy while the primary tumor is left in situ. Assessment of biological aggressiveness of the cancer without removing it would, therefore, be valuable. International consensus conferences on breast carcinoma have directed time and again to include prognostic factors in histopathology and cytology reports. ,
| > Significance of cytological grading|| |
Cytoprognostic score on FNA smear is a great promise as a cost-effective way to predict biological behavior of breast carcinoma. Evaluation of cytological tumor grade is quick, easy to perform, and correlates well with tissue nuclear grade. It is a fundamental cytologic parameter which should be included in the FNA report. FNA with cytoprognostic score can be used as a semi-quantitative alternative or additional tool in continuous monitoring of therapy effect during treatment. FNA can provide information about intrinsic features of the tumor as well as its prognosis. Considerable limitation of FNA is to differentiate between intraductal and invasive carcinoma, as a diagnosis of intraductal neoplasia requires the careful study of overall architecture and basement membrane integrity that only histopathology can provide. ,,,[35
| > Cytological reporting categories for breast lesions|| |
NHS breast screening program directs to classify the breast aspirate in five different categories. As per the recommendation of Bethesda conference, the classification of breast FNA falls into one of the five categories: Unsatisfactory smears, benign, atypical/intermediate, suspicious for malignancy and malignant. Cytopathologists have investigated the potential of useful prognostic indicators on breast aspirates. The various features taken into consideration are: Cellular morphology and arrangement, nuclear character, number of mitosis, and background. ,,,,,,,,,,,,,,,
Mouriquand and Pasquier took for scoring purpose the most anaplastic cells among the double malignant cell population into account.  Strong points about the study: (1) Correlated with high-risk patient segregation for early relapse at the time of FNA.  (2) Showed disease-free interval was inversely proportional to higher tumor grade (3) Concordant with Bloom and Richardson's histological grading.  Weak points about the study were that it was difficult to score and had low specificity. 
Black's nuclear grading scheme  did not gain popularity in the proposed original form due to the complexity; as Grade 1 equaled to anaplasia, while Grade 4 was the best differentiated. Hence, it was simplified by Fisher into three nuclear grades, with Grade 1 representing the highest level of differentiation and Grade 3 equivalent to anaplasia. Dabbs  used Fisher's modification in their study by grouping together of Grades 1 and 2 as "favorable nuclear grade," for they were prognostically similar (and favorable), while Grade 3 as "unfavorable nuclear grade" with poorer prognosis. The strengths of this system were: (1) Nuclear grade was the most powerful predictor of tumor aggressiveness, when combined with histologic tumor type and race of the patient.  Weak points were: (1) It reflected only cytological and not the architectural aspect of FNA smears. (2) Nuclear size was variable, even within similar preparations because the degree of unavoidable air-drying varied. (3) Time consuming so not widely used. (4) Subjective method as compared to objective results provided by flow cytometry.
Robinson et al. developed a protocol in 1994 for cytologic grading of IDC NOS.  This method had three cytological grades like Elston's MRB method for histological grading.  The strengths of this system included: (1) All cytological features included in the score were equally important in regression analysis which corresponded well with the established histological grades. (2) Nucleolar presence and character were valuable in grading; both independently and in combination with the other cytological features. The only weakness was that the mitotic count was not considered. 
Howell et al.  applied SBR grading system  with modifications on FNA smears. Tubule formation was identified not only by the presence of microacini, but also by the recognition of branching, elongated, three-dimensional tubular structures. The latter is similar in concept to the three-dimensional follicle seen in thyroid aspirates and consists of a sac-like or tubular structure with well-defined borders and a syncytial arrangement of overlapping nuclei.  Similar evidence of glandular differentiation has been used in grading prostate cancers.  Regarding mitoses, the threshold for a number of mitoses for each point in scoring system was arbitrarily lowered because mitoses are seen less frequently in aspirates than in surgical biopsy material. Strength of this scheme was that for all the aspects were studied, cytological grade was more predictable and reproducible and showed greater correlation between the cytological and histological specimens than score. Weakness: Discrepancies between cytologic and histologic grade due to difficulty in identification of mitoses and tubules which were not necessarily discernable in the aspirated material. In a recent study, refinement in application technique of these criteria allowed Bansal et al.  to more accurately grade the cytologic specimens.
The categorization of DS by Yu  into three groups although, appeared new, but the concept was originally given by Mouriquand et al.  in 1986 in his cytoprognostic classification, where he denoted score of 3 to isolated cells and score 0 to cells in clusters. Strength: (1) Statistically significant relationship was demonstrated between largely dyscohesive tumor cell population and distant metastasis. (2) Method of slide fixation and staining did not pose a problem as Papanicolaou-stained and rapid Romanowsky smears were equally useful for determining DS. Weakness: (1) No mention of a combined grade on summation of two features studied, that is, cellular DS and nuclear grading. (2) No correlation of cellular dyscohesive degree with regional metastases. (3) No significant relationship was found between nuclear grade and cellular cohesion. (4) Mechanical differences in smearing technique among individuals affect DS. (5) Difference in DS in areas within the same slide and between slides and gave false high DS in cases of high grade DC1S, in particular the comedo subtype. 
Study by Taniguchi et al.;  strengths: (1) Cytologic grade did correlate positively with histologic grade and negatively with estrogen receptor (ER). (2) High cytologic grade was associated with nodal metastasis and proliferative index labeling by MIB-1. (3) Necrosis was taken into consideration. (4) Showed significant clinicopathological correlation. Weakness: (1) Has not been worked upon by any other study group in literature. (2) Cell distribution pattern and mitosis were not considered.
Study by Khan et al.;  Strengths: (1) Demonstrated nuclear size in isolation as a statistically significant criterion. (2) Showed pleomorphism, plays a discriminatory role. Weakness: (1) Degree of smear cellularity did not show statistically significant correlation with the histological grade. (2) Cell dispersion criterion was difficult to assess as there were significant variations in the degree of dispersion in each smear.
Strength of the study by Fan et al.  (2006): (1) High cytoprognostic score correlated with more lymph node metastasis, and poor expression of prognostic markers (ER, progesterone receptor). (2) Cytoscore correlated well with the subsequent histological grade. Weakness: (1) Time consuming. (2) Not easily reproducible.
| > Conclusion|| |
Nuclear cytomorphological features are important prognostic markers and have been considered by all the studies for breast carcinoma grading. Among all the discussed grading systems, we suggest grading system by Howell would be most appropriate and closest to the accepted Histologic grading system as it applies SBR histological grading system  with modifications on FNA smears. We recommend it to be followed by all cytopathologists, in order to bring uniformity in the reporting of breast FNAs for grading the malignant lesions. We propose that the sign out of all breast FNAs from malignant lesions should include the cytologic grading as well, especially in low-resource settings where core biopsy is not routinely performed for diagnosis, and the treatment is often based on cytology report itself. This would provide relevant predictive and prognostic information to the attending clinician and assist him/her with better management of the patients.
| > References|| |
Rosai J. Ackerman's Surgical Pathology. 9 th
ed. Edinburgh: Mosby; 2004. p. 1787-839.
Kaufman Z, Shpitz B, Shapiro M, Rona R, Lew S, Dinbar A. Triple approach in the diagnosis of dominant breast masses: Combined physical examination, mammography, and fine-needle aspiration. J Surg Oncol 1994;56:254-7.
Steinberg JL, Trudeau ME, Ryder DE, Fishell E, Chapman JA, McCready DR, et al.
Combined fine-needle aspiration, physical examination and mammography in the diagnosis of palpable breast masses: Their relation to outcome for women with primary breast cancer. Can J Surg 1996;39:302-11.
Silverman JF, Elsheikh TM, Singh HK. The role of fine needle aspiration cytology of the breast in the core biopsy era. Pathol Case Rev 2007;12:44-8.
Berner A, Davidson B, Sigstad E, Risberg B. Fine-needle aspiration cytology vs. core biopsy in the diagnosis of breast lesions. Diagn Cytopathol 2003;29:344-8.
Silverman JF. Diagnostic accuracy, cost-effectiveness, and triage role of fine-needle aspiration biopsy in the diagnosis of palpable breast lesions. Breast J 1995;1:3-8.
Hatada T, Ishii H, Ichii S, Okada K, Fujiwara Y, Yamamura T. Diagnostic value of ultrasound-guided fine-needle aspiration biopsy, core-needle biopsy, and evaluation of combined use in the diagnosis of breast lesions. J Am Coll Surg 2000;190:299-303.
Kaufmann M, von Minckwitz G, Mamounas EP, Cameron D, Carey LA, Cristofanilli M, et al.
Recommendations from an international consensus conference on the current status and future of neoadjuvant systemic therapy in primary breast cancer. Ann Surg Oncol 2012;19:1508-16.
Schwartz GF, Hortobagyi GN, Masood S, Palazzo J, Holland R, Page D, et al.
Proceedings of the consensus conference on neoadjuvant chemotherapy in carcinoma of the breast, April 26-28, 2003, Philadelphia, PA. Hum Pathol 2004;35:781-4.
The uniform approach to breast fine-needle aspiration biopsy. National Cancer Institute Fine-Needle Aspiration of Breast Workshop Subcommittees. Diagn Cytopathol 1997;16:295-311.
Mouriquand J, Pasquier D. Fine needle aspiration of breast carcinoma: A preliminary cytoprognostic study. Acta Cytol 1980;24:153-9.
Fisher ER, Redmond C, Fisher B. Histologic grading of breast cancer. Pathol Annu 1980;15:239-51.
Hunt CM, Ellis IO, Elston CW, Locker A, Pearson D, Blamey RW. Cytological grading of breast carcinoma - A feasible proposition? Cytopathology 1990;1:287-95.
Robinson IA, McKee G, Nicholson A, D'Arcy J, Jackson PA, Cook MG, et al.
Prognostic value of cytological grading of fine-needle aspirates from breast carcinomas. Lancet 1994;343:947-9.
Yu GH, Cajulis RS, De Frias DV. Tumor cell (dys) cohesion as a prognostic factor in aspirate smears of breast carcinoma. Am J Clin Pathol 1998;109:315-9.
Taniguchi E, Yang Q, Tang W, Nakamura Y, Shan L, Nakamura M, et al.
Cytologic grading of invasive breast carcinoma. Correlation with clinicopathologic variables and predictive value of nodal metastasis. Acta Cytol 2000;44:587-91.
Khan MZ, Haleem A, Al Hassani H, Kfoury H. Cytopathological grading, as a predictor of histopathological grade, in ductal carcinoma (NOS) of breast, on air-dried Diff-Quik smears. Diagn Cytopathol 2003;29:185-93.
Bloom HJ, Richardson WW. Histological grading and prognosis in breast cancer; a study of 1409 cases of which 359 have been followed for 15 years. Br J Cancer 1957;11:359-77.
Dabbs DJ. Role of nuclear grading of breast carcinomas in fine needle aspiration specimens. Acta Cytol 1993;37:361-6.
Howell LP, Gandour-Edwards R, O'Sullivan D. Application of the Scarff-Bloom-Richardson tumor grading system to fine-needle aspirates of the breast. Am J Clin Pathol 1994;101:262-5.
Fan F, Namiq AL, Tawfik OW, Thomas PA. Proposed prognostic score for breast carcinoma on fine needle aspiration based on nuclear grade, cellular dyscohesion and bare atypical nuclei. Diagn Cytopathol 2006;34:542-6.
Mouriquand J, Gozlan-Fior M, Villemain D, Bouchet Y, Sage JC, Mermet MA, et al.
Value of cytoprognostic classification in breast carcinomas. J Clin Pathol 1986;39:489-96.
Black MM, Speer FD. Nuclear structure in cancer tissues. Surg Gynecol Obstet 1957;105:97-102.
Weidner N, Cady B, Goodson WH 3 rd
. Pathologic prognostic factors for patients with breast carcinoma. Which factors are important. Surg Oncol Clin N Am 1997;6:415-62.
Chang J, Clark GM, Allred DC, Mohsin S, Chamness G, Elledge RM. Survival of patients with metastatic breast carcinoma: Importance of prognostic markers of the primary tumor. Cancer 2003;97:545-53.
Latinovic L, Heinze G, Birner P, Samonigg H, Hausmaninger H, Kubista E, et al.
Prognostic relevance of three histological grading methods in breast cancer. Int J Oncol 2001;19:1271-7.
Elston CW. Grading of invasive carcinoma of the breast. In: Page DL, Anderson TJ, editors. Diagnostic Histopathology of the Breast. London New York: Churchill Livingstone; 1987. p. 300-11.
Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: Experience from a large study with long-term follow-up. Histopathology 1991;19:403-10.
National Institutes of Health Consensus Development Panel. National Institutes of Health Consensus Development Conference Statement: Adjuvant therapy for breast cancer, November 1-3, 2000. J Natl Cancer Inst Monogr 2001;30:5-15.
Blamey RW, Ellis IO, Pinder SE, Lee AH, Macmillan RD, Morgan DA, et al.
Survival of invasive breast cancer according to the Nottingham prognostic index in cases diagnosed in 1990-1999. Eur J Cancer 2007;43:1548-55.
Cardoso F, Costa A, Norton L, Cameron D, Cufer T, Fallowfield L, et al
. 1 st
International consensus guidelines for advanced breast cancer (ABC 1). Breast 2012;21:242-52.
van Diest PJ, Mouriquand J, Schipper NW, Baak JP. Prognostic value of nucleolar morphometric variables in cytological breast cancer specimens. J Clin Pathol 1990;43:157-9.
Ciatto S, Bonardi R, Herd-Smith A, Cariaggi P, Confortini M, Bulgaresi P. Prognostic value of breast cancer cytologic grading: A retrospective study of 213 cases. Diagn Cytopathol 1993;9:160-3.
Ishikawa T, Hamaguchi Y, Tanabe M, Momiyama N, Chishima T, Nakatani Y, et al.
False-positive and false-negative cases of fine-needle aspiration cytology for palpable breast lesions. Breast Cancer 2007;14:388-92.
Bonzanini M, Gilioli E, Brancato B, Cristofori A, Bricolo D, Natale N, et al.
The cytopathology of ductal carcinoma in situ
of the breast. A detailed analysis of fine needle aspiration cytology of 58 cases compared with 101 invasive ductal carcinomas. Cytopathology 2001;12:107-19.
Silverman JF. Breast. In: Bibbo M, editor. Comprehensive Cytopathology. 2 nd
ed. Philadelphia, PA: Saunders; 1997. p. 770.
Sneige N, Staerkel GA, Caraway NP, Fanning TV, Katz RL. A plea for uniform terminology and reporting of breast fine needle aspirates. M.D. Anderson cancer center proposal. Acta Cytol 1994;38:971-2.
Das AK, Kapila K, Dinda AK, Verma K. Comparative evaluation of grading of breast carcinomas in fine needle aspirates by two methods. Indian J Med Res 2003;118:247-50.
Fisher ER, Redmond C, Fisher B, Bass G. Pathologic findings from the National Surgical Adjuvant Breast and Bowel Projects (NSABP). Prognostic discriminants for 8-year survival for node-negative invasive breast cancer patients. Cancer 1990;65:2121-8.
Robles-Frías A, González-Cámpora R, Martínez-Parra D, Robles-Frías MJ, Vázquez-Cerezuela T, Otal-Salaverri C, et al.
Robinson cytologic grading of invasive ductal breast carcinoma: Correlation with histologic grading and regional lymph node metastasis. Acta Cytol 2005;49:149-53.
Kini SR. Guides to clinical aspiration biopsy: Thyroid. Diagn Cytopathol 1991;7:215-6.
Maksem JA, Johenning PW. Is cytology capable of adequately grading prostate carcinoma? Matched series of 50 cases comparing cytologic and histologic pattern diagnoses. Urology 1988;31:437-44.
Bansal C, Singh US, Misra S, Sharma KL, Tiwari V, Srivastava AN. Comparative evaluation of the modified Scarff-Bloom-Richardson grading system on breast carcinoma aspirates and histopathology. Cytojournal 2012;9:4.
Schiller AB, Tadros TS, Birdsong GG, Grossl NA. Cellular dyscohesion in fine-needle aspiration of breast carcinoma. Prognostic indicator for axillary lymph node metastases? Am J Clin Pathol 2001;115:219-23.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]