|Year : 2011 | Volume
| Issue : 2 | Page : 240-245
Evaluation of scoring system in cytological diagnosis and management of breast lesion with review of literature
NM Nandini, TS Rekha, GV Manjunath
JSS Medical College, JSS university, Mysore, India
|Date of Web Publication||11-Jul-2011|
N M Nandini
JSS Medical College, JSS university, Mysore
Source of Support: None, Conflict of Interest: None
Background: Fine needle aspiration cytology (FNAC) breast is generally considered as a rapid, reliable, and safe diagnostic tool to distinguish non-neoplastic from neoplastic breast lesions. Masood's Scoring Index has been proposed to help in sub-grouping of breast lesions so as to help in surgical management. Aims: To assess the accuracy of Modified Masood's Scoring Index (MMSI) in the diagnosis of benign and malignant breast lesions in patients with palpable breast lump, and review of literature. Settings and Design: A prospective study from a tertiary care center. Material and Methods: This prospective study included a total of 100 cases, both females and males, with palpable breast lump, in the age range of 10-80 years, over a period of 2 years from January 2007 to 2009, who underwent FNAC. They were cytologically grouped into five categories as suggested by Masood et al, and confirmed by histopathology. Results: Evaluation of Masood Scoring Index led to modification (Modified Masood Scoring Index; MMSI) by shifting score 9 from Group I to Group II, thus increasing the diagnostic accuracy of the breast lesions. Conclusions: MMSI was found to be a useful, easily reproducible scoring method of breast lesions to improve diagnostic accuracy of nonproliferative breast disease and proliferative breast disease without atypia cases, as the prognosis and treatment of these cases varies.
Keywords: Biopsy, breast aspiration, cytology, Modified Masood Scoring index
|How to cite this article:|
Nandini N M, Rekha T S, Manjunath G V. Evaluation of scoring system in cytological diagnosis and management of breast lesion with review of literature. Indian J Cancer 2011;48:240-5
|How to cite this URL:|
Nandini N M, Rekha T S, Manjunath G V. Evaluation of scoring system in cytological diagnosis and management of breast lesion with review of literature. Indian J Cancer [serial online] 2011 [cited 2021 Jan 22];48:240-5. Available from: https://www.indianjcancer.com/text.asp?2011/48/2/240/82891
| » Introduction|| |
The technique of fine needle aspiration cytology (FNAC) was first described in 1847. It was introduced into clinical practice by Ellis and Martin in 1930s. , Thirty years later, it gained acceptance first in Europe and about a decade later in North America.  Cancer breast is the important and common malignant disease affecting women in the industrialized world. , It is the second most common cancer in women of the developing world. The increasing trend of its incidence in urban population of developing world is because of changing to western lifestyles. 
FNAC breast is generally considered as a rapid, reliable, and safe diagnostic tool to distinguish non-neoplastic from neoplastic breast lesions. In developed countries, in the last 20 years, mammographic scoring programs, which have been used extensively, are designed to detect the earliest possible breast cancer.  Core-needle biopsy (CNB) is increasingly replacing FNAC in many centers in developed countries and this is mainly attributed to the inability of FNAC to distinguish carcinoma in situ from invasive carcinoma.  FNAC has a role in diagnosis of palpable breast lesions in developing countries as the initial method of pathological assessment. Also, as found by different authors like Than,  Zagorianaku et al, and Koss et al, FNAC of palpable breast lesions is a component of Triple test. Also, factors like low cost, rapid reporting and patient compliance are better for FNAC procedure, even though it has limitations such as operator efficiency and the need of experienced medical staff. , Epithelial hyperplasia, a component of proliferative breast disease (PBD), is a known risk factor for the development of breast carcinoma. , The risk of breast carcinoma in cases of PBD without atypia is 1.3 times and in PBD with atypia is 4.3 times. 
FNAC breast has taken a fundamental role in the diagnosis of both palpable and non-palpable lesions using ultrasound or stereotactic guidance as it gives the necessary information of the various breast lesions for the surgical management of patients. ,,,
As the prognosis and thereby the line of management of each group of breast lesions varies, it is important to recognize the spectrum of morphological changes seen and separate them into benign, premalignant and malignant categories. 
Masood et al,  developed a cytological grading system to delineate these categories based on the cellular arrangement (relationship of cells to one another in a sheet of ductal epithelial cells), the degree of cellular pleomorphism (the variation in cell size of the ductal epithelial cells), anisonucleosis, the presence of myoepithelial cells, nucleoli and the status of chromatin pattern like clumping of chromatin. Values ranging from 1 to 4 were assigned to each criterion, and a score based on the sum of the individual values was calculated for each case. The scores ranged from a minimum of 6 to a maximum of 24. The cases were divided on cytological basis into nonproliferative breast disease (NPBD), PBD without atypia, PBD with atypia and carcinoma. Comparing the cytological diagnosis to histopathology diagnosis, they found a high degree of concordance between the results. We, the authors, over a 2-year period, evaluated 100 palpable lesions using these criteria and after correlating with their histopathology found that diagnostic accuracy can be further achieved by shifting score 9 and score 10 from NPBD to PBD without atypia. Thus, NPBD becomes score 6-8 and PBD without atypia becomes score 9-14. We have designated this as Modified Masood's Scoring Index (MMSI) [Table 1], [Table 2].
|Table 1: Grading system for interpretation of FNAB (Masood's Scoring Index) |
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|Table 2: Cytologist criteria/grading system for interpretation of FNAB breast (Modified Masood's Scoring Index) |
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The scoring systems proposed by Page et al and Dawson AE et al have consistently found that architectural features like three-dimensional epithelial clusters, swirling or streaming of intraluminal cells and peripheral slit-like irregular lumen helped to differentiate PBD without atypia from ductal carcinoma insitu (DCIS), the findings which were supported by Sneige and Staerkel.  Most studies for scoring of breast lesions use traditional cytologic features that include cellularity, nuclear pleomorphism, overlap and loss of polarity. ,,, Scoring indices for malignant breast lesions have been proposed by many authors like Hunt,  Zajdala,  Black,  Moriquand,  Layfield  and Robinsons  which have also used cytological and nuclear features of breast lesions for grading of malignancy.
| » Materials and Methods|| |
A total of 100 cases, both males and females, with palpable breast lumps and in age group of 10-80 years, over a period of 2 years from January 2007 to 2009, were included in the study. After the palpable breast lumps were fixed between thumb and index finger, 22 gauze needle attached to a 10 ml syringe was inserted into the lump, and suction pressure was applied by withdrawing the syringe plunger to 2 ml mark. Three to four passes were made into the substance of the lump, keeping the needle within the breast at all times. The needle was withdrawn and the aspirate expressed and thinly spread on four to five clean dry glass slides. Hematoxylin-eosin and PAP stains were used for the slides which were fixed in 95% ethyl alcohol. Air-dried smear was stained with May-Grunwald Giemsa stain. One slide was stained by Toluidine blue rapid stain to see for adequacy. Criteria for adequacy were the presence of four to five clusters of ductal epithelial cells, each made up of five to six cells with presence of a few bare benign nuclei in the background. Three cases were inadequate on repeated aspiration for reporting and were advised biopsy.
Of the 100 cases, 97 were females and 3 were males. Cytological diagnosis and MMSI was done by independent observers. The scores were compared and in cases differing by more than 2 scoring points, the slides were reviewed and findings were corrected.
| » Results|| |
The patients included in the study were both females and males in the age range of 10-80 years. The maximum number of cases was in the age group of 31-40 years, totaling to 35 cases. Sex ratio (Female:Male) was 32:1. We classified the breast lesions into five groups based on cytological diagnosis [Table 3].
|Table 3: Comparison table of cytologically classified groups with MMSI and histopathological diagnosis |
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Nonproliferative breast disease (Group I)
Cytological features of this group include monolayering of uniform sized cells, monomorphic cellular arrangement and presence of myoepithelial cells. Nuclear features include absence of anisonucleosis, nucleoli and chromatin clumping. Background shows fibromyxoid stroma with occasional cases showing cyst macrophages and apocrine change [Figure 1].
|Figure 1: (a) Nonproliferative breast disease (NPBD) (MMSI-8) smear shows monotonous population of benign ductal epithelial cells with myoepithelial cells in the background (H and E, ×400). (b) The corresponding histopathology (H and E, ×200)|
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The total number of wcases of fibroadenoma (FA) was 31/100. Number of cases of FA with atypia on cytology was 8, totaling to 39/100. Number of cases of FA and FA with atypia which turned out to be PBD without atypia by MMSI and HPE was 18. Of these, 9/18 cases had a score of 9 by Masood's scoring system, i.e., 50% of the cases shifted to PBD without atypia. Number of cases where both the observers gave the same score was 22/39 (55%).
Proliferative breast disease without atypia (Group II)
The cytological features of this group include moderate to high cellularity, mild cellular pleomorphism, and decrease in number of myoepithelial cells. There is mild nuclear overriding with occasional micronucleoli and chromatin clumping. Background shows apocrine cells, cyst macrophages and occasional bare nuclei [Figure 2].
|Figure 2: (a) Proliferative breast disease without atypia (PBD without atypia) (MMSI-10). Smear shows sheets of ductal epithelial cells with mild cellular pleomorphism, nuclear overlapping and occasional prominent nucleoli (PAP, ×400). Background shows myoepithelial cells. (b) The corresponding histopathology (H and E, ×200)|
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Number of cases of PBD without atypia diagnosed cytologically was 23/100. To these, 18 cases from Group I (NPBD) were added. Number of cases where both the observers gave the same score was 16/23 (66%). Number of cases with score 9 was 10/23. Of the 18 cases which were added to this group, 9/18 had score 9, i.e., total of 19/41 had score 9 (50% of cases) in Group II.
Proliferative breast disease with atypia (Group III)
Even though this group had fewer cases than PBD without atypia, Group III has cytomorphologic features which overlap with carcinoma. It presents with moderate to high degree of cellularity, moderate degree of cellular pleomorphism and anisonucleosis.
The nuclear features include significant increase in the number of micronucleoli and chromatin clumping, a few myoepithelial cells and decrease in the number of bare benign nuclei [Figure 3]. Number of cases diagnosed cytologically was 3/100. One case was diagnosed as carcinoma breast by MMSI, which was confirmed by histopathology.
|Figure 3: (a) Proliferative breast disease with atypia (PBD with atypia) (MMSI-15). Smear shows sheets of ductal epithelial cells with moderate degree of cellular pleomorphism, nuclear overlapping and occasional prominent nucleoli (H and E, ×400). (b) The corresponding histopathology (H and E, ×200)|
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Carcinoma breast (Group IV)
This group shows cytological features characterized by loosely arranged cellular pattern, high cellularity, nuclear pleomorphism, chromatin clumping with macronucleoli and absence of myoepithelial cells. Background shows necrosis and hemorrhage [Figure 4]. Number of cases diagnosed on cytology was 29/100. All the cases correlated with histopathology. In 16/29 cases (53%), both the observers gave the same score.
|Figure 4: (a) Sheets of highly pleomorphic cluster of ductal epithelial cells with single tumor cells in the background, absence of myoepithelial cells (H and E, ×400). (b) The corresponding histopathology (H and E, ×200)|
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Non-neoplastic and miscellaneous lesions (Group V)
This had 6/100 cases which include three cases of scanty aspirate, two cases of simple cyst and one case of inflammatory breast lesion.
| » Discussion|| |
FNAC of breast is a well-established modality for the investigations of palpable breast lumps as well as non-palpable breast lesions detected on mammography. ,,,,,,
It is generally agreed that NPBD has mild risk (1.5-2 times) and PBD with atypia has moderately increased risk (4-5 times) of breast cancer. Patients who have carcinoma in situ have 8-10 times risk of breast cancer. ,,, Therefore, it is necessary that an accurate diagnosis on cytology be offered.
Histopathological criteria that allow the distinction of these proliferative lesions have been established. A number of articles have been published on the cytology of PBD, taking cytological and nuclear features into consideration, such as those of Masood et al, Sneige et al, Frost, Thomas et al, Pandhey and Dzuira et al. ,,,,, Of these, we have studied the criteria put forth by Masood et al. 
We have found the six cytological parameters proposed by Masood et al,  which are useful for cytological scoring of breast lesions. We found that to increase the accuracy of various groups, the scoring index be slightly modified; NPBD, which had score of 6-10, was modified to score of 6-8 with shift of score 9 and 10 to PBD without atypia, i.e., score 11-14 is modified to score 9-14.
This is important as the prognosis of Group II differs form Group I and has slightly increased risk. It was found that a few architectural features were consistently observed in cases of PBD. It includes three-dimensional epithelial clusters, swirling or streaming of intraluminal cells and peripheral, slit-like, irregular sub-lumens.
A few workers like Sneige and Staerkel  compared architectural features in FNA of ductal hyperplasia and ductal carcinoma in situ, and also the cytological scoring system of Masood's which we have followed in our study.
Even though Sneige and Staerkel  concluded that the architectural features were more useful for diagnosis of PBD, we found that in addition, cytological and nuclear features were helpful to distinguish these cases, as suggested by Dawson et al. 
PBD with atypia (Group III)
This group is important to identify, as it almost leads to malignancy and there are cytological features which overlap between PBD without atypia, PBD with atypia and low-grade carcinoma of breast. ,,, Besides cytological and architectural findings, many workers found that the six parameters of MMSI have helped in diagnosis of these cases a nd vice versa, ,, as was observed in one case in the present study. It was diagnosed as PBD with atypia on cytology, but on scoring and histopathology, it turned out to be a low-grade carcinoma breast.
Some authors , have found that PBD falls into a spectrum of lesions that increase in severity to ductal carcinoma in situ and carcinoma, as was found in our study where cytology showed the full spectrum of NPBD, PBD with atypia to carcinoma breast which was confirmed by MMSI and histopathology.
Carcinoma breast (Group IV)
The carcinoma breast group includes 29 cases confirmed by MMSI and histopathology. Various methods of cytological and nuclear grading of breast carcinoma have been advocated by Zajdela,  Hunts,  Layfield,  Black,  Moriquand et al and Robinsons.  MMSI can be compared with Robinson's grading system as both have cellular and nuclear features for grading the breast carcinoma.
The Group V by cytological classification has six cases in which MMSI could not be used. Limitation observed in implementation of MMSI is inflammation which falsely increases the scoring due to nuclear atypia. Inadequate aspirate and dark nuclear staining interfere with proper scoring. Benign and malignant breast subtypes cannot be diagnosed by scoring system.
By this study, we infer that the histopathology criteria developed for the diagnosis of breast lesions can be applied to breast FNAC. FNAC helps to diagnose and categorize different breast lesions like NPBD, PBD without atypia, PBD with atypia and malignancy. Cytological methods have been proposed by various authors, of which we have utilized Masood's scoring index and slightly modified it by shifting score 9 and 10 from Group I to Group II. This helps in increasing the diagnostic accuracy and decides the line of management of cases. MMSI has its best use in accurate diagnosis of cytological NPBD and PBD without atypia cases. MMSI is a cost-effective method of identifying women with an increased risk for subsequent invasive breast cancer.
| » Conclusions|| |
MMSI was found to be a useful, easily reproducible scoring method of breast lesions and can be used to improve diagnostic accuracy of NPBD and PBD without atypia cases, as the prognosis and treatment of these cases varies.
| » Acknowledgment|| |
JSS Medical College, constituent college of JSS University, Mysore, is acknowledged.
| » References|| |
|1.||Bowa K, Jewel J, Mudenda V. Fine needle aspiration cytology in the investigation of breast lumps at the University Teaching Hospital in Lusaka, Zambia. Trop Doct 2008;8:245-7. |
|2.||Zagorianakou P, Fiacequentos, Zagorianakou N, Makrydimas G, Stefanou D, Agnantis NJ. FNAC: Its roles limitations and prospective in the preoperative diagnosis of breast cancer. Eur J Gynaecol Oncol 2005;26:143-9. |
|3.||Koss LG, Melamed MR. The breast. In: Koss LG, Melamed MR, editors. Koss's Diagnostic Cytology and its Histopathologic Basis. New York: Lippincott Williams and Wilkins; 2006. p. 1081-147. |
|4.||Bhatt JV, Shah JM, Shah FS. Pathophysiology of breast lesions: Vision beyond the clinical eye. J Appl Basic Med Sci 2002;4:81-4. |
|5.||Tham TM, Iyengar KR, Taib NA, Yip CH. Fine needle aspiration biopsy, core needle biopsy or excision biopsy to diagnose breast cancer-which is the ideal method? Asian Pac J Cancer Prev 2009;10:155-8. |
|6.||Dawson AE, Mulford DK, Sheils LA. The cytopathology of Proliferative breast disease comparision with ductal carcinoma in situ. Am J Clin Pathol 1995;103:438-42. |
|7.||Dupont WD, Parl FF, Hartmann WH, Brimton LA, Winfield AC, Worrell JA, et al. Breast cancer risk associated with proliferative breast disease and atypical hyperplasia. Cancer 1993;71:1258-65. |
|8.||Mirdha AR, Iyer VK, Kapila K, Verma K. Value of Scoring System in classification of proliferative breast disease on fine needle aspiration cytology. Indian J Pathol Microbiol 2006;49:334-40. |
|9.||Khan N, Afroz N, Rana F, Khan MA. Role of cytologic grading in prognostication of invasive breast carcinoma. J Cytol 2009;26:65-8. |
|10.||Masood S. Cytomorphology of fibrocystic change, high-risk proliferative breast disease and premalignant breast lesions. Clin Lab Med 2005;25:713-31. |
|11.||Page DL, Dupont WD, Rogers LW, Rados MS. Atypical hyperplastic lesions of the female breast: A long term follow-up study. Cancer 1985;55:2698-708. |
|12.||Sneige N, Staerkel GA. Fine needle aspiration Cytology of Ductal hyperplasia with and without atypia and ductal carcinoma in situ. Hum Pathol 1994;25:485-92. |
|13.||Dziura BR, Bonfiglio TA. Needle cytology of the breast: A study of the cells of benign and malignant ductal neoplasia. Acta Cytol 1979;23:332-40. |
|14.||Bibbo M, Scheiber M, Cajulis R, Keebler CM, Wied GL Dowlatshashi K. Stereotaxic fine needle aspiration cytology of clinically occult malignant and premalignant breast lesions. Acta Cytol 1988;32:193-201. |
|15.||Frost AR, Tabbara SO, Poprocky LA, Weiss H, Sidawy MK. Cytologic features of proliferative breast disease. A study designed to minimize sampling error. Cancer (Cancer cytopathol) 2000;90:33-40. |
|16.||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. |
|17.||Zajdela A, DelaRiva J, Gossein N. The relation of prognosis to the nuclear diameter of breast cancer cells obtained by cytologic aspiration. Acta Cytol 1979;23:75-80. |
|18.||Black MM, Spees FD. Nuclear structures in Cancer tissues. Surg Gynaecol Obstet 1957;105:97. |
|19.||Moriguand J, Gozian - Fiorm, Villemain D, Bouchet Y, Sage JC, Munet MA, et al. Value of cytoprognostic classification in breast carcinomas. J Clin Pathol 1986;39:89-96. |
|20.||Layfield LJ, Robert EM. Aspiration biopsy smear pattern as a predictor of biological behavior in adenocarcinoma of the breast. Acta Cytol 1992;36:208-14. |
|21.||Sharma.SP, Mishra RK, Agarwal D. Comparative evaluation of nuclear grading in FNAC smears and tissue sections in cases of carcinoma breast. J Cytol 2000;17:141-7. |
|22.||Masood S, Frykberg ER, McLellan GL, Scalapino MC, Mitchun DG, Bullard JB. Prospective evaluation of radiologically directed fine needle aspiration biopsy of nonpalpable breast lesions. Cancer 1990;66:1480-87. |
|23.||Mulford DR, Dawson AE. Atypia in fine needle aspiration cytology of non-palpable and palpable mammographically detected breast lesions. Acta Cytol 1994;38:9-17. |
|24.||Karthik K, Ganapathy H, Alavander E, Devadas G. Evaluation of fine needle aspiration smears of proliferative breast lesions. J Cytol 2004;21:26-9. |
|25.||Thomas JS, Mallon EA, George WD. Semi-quantitative analysis of Fine needle aspirates from benign and malignant breast lesions. J Clin Pathol 1989;42:28-34. |
|26.||Gangopadhyay M, Nijhawan R, Joshi K, Gupta SK. Cytology of "Significant" breast ductal proliferations. Acta Cytol 1997;41:1112-20. |
|27.||Masood S, Hardy NM, Assaf N, Lul. Cytological grading system in diagnosis of high risk and malignant breast lesions. Merits and Pitfalls. Acta Cytol 1994;38:798. |
|28.||Lindholm K. Breast. In: Orell SR, Sterrett GF, Whitaker D, editors. Fine needle aspiration cytology. Australia: 2005. p. 165-225. |
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3]
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