Secondary Logo

Journal Logo

The diagnostic role of fine-needle aspiration cytology combined with ultrasonography in cystic breast lesions

Abdallah, Dina M.a; Fayed, Haytham M.b; Ibrahim, Mohamed G.b; Fawzy, Rawya K.c; Sadek, Rehab H.b

doi: 10.1097/01.XEJ.0000455922.95785.09
ORIGINAL ARTICLES
Free

Background Breast cysts are among the more common reasons for referral to a breast clinic. They may be detected incidentally on screening mammography or patients may present with symptoms and signs such as mastalgia, nipple discharge, or a palpable mass. Breast ultrasound plays an established role in the evaluation of breast abnormalities, especially in women under 40 years of age. Fine-needle aspiration cytology (FNAC) has become a popular and valuable tool in the preoperative assessment of breast masses, and it shows a high accuracy, sensitivity, and specificity. The triple-diagnostic method (consisting of clinical evaluation, mammography, and FNAC) yields a precise diagnosis and reduces the risk of missed diagnosis of breast cancer to less than 1%.

Aim The aim of this work was to evaluate FNAC for cystic breast lesions compared with the sonographic findings and their impact on the management policy.

Patients and methods Triple assessment was carried out on 60 patients with the diagnosis of breast cysts, which included full history taking, clinical examination, ultrasonography, and FNAC.

Results The most common cystic breast lesion in the present study was fibrocystic disease (46.7%), followed by abscess (20%), and the least common lesion was fat necrosis (3.3%). Regarding the radiological classification of breast cysts, simple cysts were the most common type in this study (36 cases), there were 14 cases of complicated cysts, whereas complex cysts were the least common (10 cases). Cytological examination of simple cysts was mostly bloody or inflammatory, complicated cysts were mostly inflammatory, whereas complex cysts were mostly malignant. There was a statistically significant correlation between the cyst type and the cellular content. There was no statistically significant correlation between the cyst margin and the cellular content. Regular cyst margins had a bloody and inflammatory aspirate, whereas irregular cyst margins were either inflammatory or malignant. Histopathological examination of cysts with a residual mass after aspiration showed intracystic carcinoma (six cases), abscess (two cases), fibrocystic disease (two cases), and hematoma (two cases). This correlation was statistically significant. The correlation between the cytological study and the color of the aspirate was statistically significant; malignant cells were noted mainly in bloody or greenish aspirates, whereas yellowish aspirates were always inflammatory.

Conclusion The accuracy of sonography and fine-needle aspiration in detecting and allowing the correct diagnosis of cysts has been reported to be almost 100%. The use of sonography has reduced the number of biopsies performed for benign breast cysts. Aspiration should be followed by excisional biopsy when (a) blood or green fluid is aspirated or (b) the mass does not disappear completely.

Departments of aPathology

bSurgery, Alexandria Faculty of Medicine

cDepartment of Radiology, Institute of Health Research, Alexandria University, Alexandria, Egypt

Correspondence to Dina M. Abdallah, 20 Yehya El-Mashad Smouha, Alexandria 21431, Egypt Tel: +2034200734; e-mail: dinabdalla@yahoo.com

Received June 20, 2014

Accepted July 27, 2014

Back to Top | Article Outline

Introduction

Cystic breast disease has been recognized as the most frequent benign breast lesion in women. Up to one-third of women aged 30–50 years have cysts in their breasts. The true incidence is probably much higher than the clinically recognized cases, and the prevalence has been estimated to be between 50 and 90% (Chun et al., 2005; Mannello et al., 2006).They may be detected incidentally on screening mammography or patients may present with symptoms and signs such as mastalgia, nipple discharge, or a palpable mass (Stavros et al., 1995; Stavros, 2004).

Cystic breast disease includes all of the benign breast pathologic states, comprising dilatation of ducts and acini to form cysts, proliferation and metaplasia of their epithelial lining, and multiplication of ducts and acini to give a picture of adenosis, which, altogether, constitute the disease (Rinaldi et al., 2010).

Breast ultrasound plays an established role in the evaluation of breast abnormalities, especially in women under 40 years of age (Venta et al., 1999; Berg et al., 2003). The increasing use of ultrasound in breast diagnosis has resulted in the frequent identification of incidental benign-appearing lesions (Venta et al., 1999; Kopans, 2006). Clinicians involved in the management of women with breast abnormalities are frequently dealing with imaging findings that are not considered suspicious, but raise a small possibility of malignancy (Sartorius, 1995). Ultrasound also facilitates intervention in the form of ultrasound-guided needle biopsy, which is increasingly available and minimally invasive, and may be considered as a simple solution in terms of diagnosis and reassurance to the patient (Venta et al., 1999).

With ultrasound, breast cysts are categorized as simple, complicated, or complex. Appropriate categorization is important because the management of each type differs (Lamb et al., 2000; Cardenosa, 2007).

Simple cyst: simple cysts typically present as a smooth-bordered mobile mass. Complex cysts: a cyst with thick walls or some discrete solid component, such as septa greater than 0.5 mm thick or mural nodules. The differential diagnosis of a complex cyst includes hematoma, fat necrosis, abscess, galactocele, and necrotic neoplasm. Complicated cysts: cystic lesions containing fluid-debris levels or floating echogenic debris in addition to the clinical findings of pain, tenderness, erythema, and fever and the clinical laboratory findings of leukocytosis and an elevated sedimentation rate.

Fine-needle aspiration cytology (FNAC) has become a popular and valuable tool in the preoperative assessment of breast masses, and it shows a high accuracy, sensitivity, and specificity. It has gained popularity because it is a fast and easy approach, is inexpensive, and can be performed with few complications (Mendoza et al., 2011). FNAC is a less demanding technique than surgical biopsy, with a low risk of complications, which suits for an outpatient clinic procedure. It is easily repeatable and can be used in multiple lesions. Preoperative FNAC can cause local tissue changes, such as hematoma, infarction, capsular pseudoinvasion, and pseudomalignant reparative reactions, which could render subsequent histological diagnosis difficult (Lindholm, 2003).

Much confidence has been placed on the triple approach because it can obviate the standard excisional biopsy when all three components of the triple test are conclusively negative or positive. Nevertheless, in FNAC of breast lesions, there are instances where the differentiation of benign and malignant is not possible (Enriori et al., 1992). This problem arises when a paucity of specimen sampling is encountered or there is a morphological overlap between benign and malignant lesions (e.g. atypical hyperplasia and low-grade carcinoma in situ, or in papillary lesions). As a result and to accommodate these problematic areas, cytological reporting categories are used to describe their features objectively in cytological terms and to incorporate the groups with uncertainties (Mendoza et al., 2011).

Back to Top | Article Outline

Standardized reporting of FNAC

The most commonly used categorization is a five-tier system, with categories ranging from insufficient materials (C1), benign (C2), atypical (C3), suspicious of malignancy (C4), to frankly malignant (C5) (Table 1). This categorization helps cytopathologists to define uncertain areas and clinicians to offer further investigation such excisional biopsy judiciously (Zakhour and Wells, 1999; Mendoza et al., 2011).

Table 1

Table 1

The inadequate rate for FNAC (C1) varies widely from centre to centre. This, however, could be kept to a minimum with a dedicated and skilled team, especially where a cytopathologist is present for immediate feedback (Dennison et al., 2003).

Malignant aspirates can range from the most obvious with markedly pleomorphic tumor cells that are easily diagnosable to those with more subtle features that need to be scrutinized with utmost care. The latter include the ‘low-grade’ group such as lobular, tubular, and grade 1 ductal subtypes compounded by either a low cell yield or cohesive clustering rather than a dissociated population (Yang and Bao, 2000).

Hemorrhagic cystic fluid, particularly in older patients, needs to be processed to examine for malignant cells as carcinomas with central cystic degeneration may be encountered. In these cases, an image-directed fine-needle aspiration of the cyst wall may yield a diagnostic sample (Lioe, 2007).

With the introduction of stereotactic and ultrasonographically guided methods for nonpalpable lesions, FNAC has been used more widely in the evaluation of nonpalpable breast lesions. Furthermore, the triple-diagnostic method (consisting of clinical evaluation, mammography, and FNAC) yields a precise diagnosis and reduces the risk of missed diagnosis of breast cancer to less than 1% (Lioe, 2007). False-negative and false-positive cases can be kept to a minimum with good correlation with clinical and radiological findings (Gao et al., 2005).

The aim of this work was to evaluate FNAC for cystic breast lesions compared with their sonographic findings and their impact on the management policy.

Back to Top | Article Outline

Patients and methods

The study included 60 patients with the clinical and radiological diagnosis of cystic breast lesions. They underwent clinical, sonographic, and fine-needle aspiration study in the Main Hospital of Alexandria University and Alexandria Police Hospital after obtaining their informed consent. Data were approved by the Alexandria Faculty of Medicine ethics committee.

Back to Top | Article Outline

Results

The youngest patient was 17 years old and the oldest was 64 years old, with a mean age of 35+12 years. A positive family history of breast cysts was detected in 70% of the cases, whereas a history was not present in 30% of the cases. Bilateral affection was found in 30% of the cases, whereas unilateral affection was present in 70% of them. The left breast had the highest incidence in unilateral cases, at 43.3%, and the remaining 26.7% were in the right breast. About 40% of the cysts occurred in the upper outer quadrant. The next most common site was the lower outer quadrant, in 23.3% of the cases. This was followed by the upper inner quadrant (16.7%), and then both the lower inner and the axillary tail at an equal incidence of 10%.

The ultrasonographic study revealed that 70% of the cysts were single, whereas 30% were multiple. There were 36 simple cysts, 14 cases of complicated cysts, and only 10 cases of complex cysts (Fig. 1).

Fig. 1

Fig. 1

The amount of aspirate obtained in the study did not exceed a volume of 5 ml. Most of the cysts (40%) yielded a volume of 2 ml regardless of the size of the cyst. About 20% yielded 3 ml and another 20% yielded 4 ml. The smallest volume was 1 ml and that was obtained from 13.3% of the cysts, whereas the largest volume was 5 ml and was obtained from 6.7% of the cysts.

Regarding the color of the aspirate, most of the cysts yielded a yellowish tinged fluid (40% of the cases), and a brownish fluid was aspirated from 23.3% of the cysts. A bloody aspirate was obtained from 20% of the cysts. Galactoceles yielded a milky aspirate (10%), and 6.7% of the cysts yielded a greenish fluid.

Cytological examination of the simple cysts revealed the following: 14 cysts were acellular, 12 had red blood cells (RBCs), whereas inflammatory cells and ductal cells were found in six and four cases, respectively (Figs 2–4). Complicated cysts mostly had inflammatory cells (10 cysts), whereas of the remaining four cysts, two had malignant ductal cells and two had RBCs. Regarding the complex cysts, they varied between malignant cells (Figs 5–7) and inflammatory cells (four cases each), whereas the remaining two cysts had RBCs admixed with benign ductal cells.

Fig. 2

Fig. 2

Fig. 3

Fig. 3

Fig. 4

Fig. 4

Fig. 5

Fig. 5

Fig. 6

Fig. 6

Fig. 7

Fig. 7

There was a statistically significant correlation between the cyst type and the cellular content (P=0.023) (Table 2).

Table 2

Table 2

About 50 cysts in the study had regular margins. Cytology of the cystic fluid showed majorly acellular fluid, RBCs, or inflammatory cells. In all, 16 of these cysts had RBCs, 14 had inflammatory cells, 14 of the cysts had an acellular content, four had benign ductal cells, and two had malignant cells. Ten of the cysts in the study had an irregular margin, six of which had inflammatory cells, whereas the other four had malignant cells.

There was no statistically significant correlation between the cyst margin and the cellular content (P=0.039) (Table 3).

Table 3

Table 3

The pathological examination of cysts with a residual mass after aspiration showed the following results: intracystic carcinoma (six cases), abscess (two cases), fibrocystic disease (two cases), and hematoma (two cases). This correlation was statistically significant (P=0.000) (Table 4).

Table 4

Table 4

The color of the aspirated cyst fluid was of the following variants: yellowish (straw colored), greenish, brownish, bloody, or milky. There were 24 cysts that yielded a yellowish aspirate in this study, 10 of which had inflammatory cells on cytological study, eight were acellular, four had RBCs, and two had ductal cells. Four cysts with a greenish aspirate had malignant cells on cytology. The brownish-colored aspirate mostly contained inflammatory cells (14 cysts), two cysts had RBCs, two had ductal cells, and two were acellular. The 12 cysts that yielded a bloody aspirate had RBCs, with two cysts having malignant cells on cytology. A milky fluid was aspirated from six cysts: two had inflammatory cells and four were acellular fluid. The correlation between the cytological study and the color of the aspirate was statistically significant (P=0.001).

Back to Top | Article Outline

Discussion

Breast cysts are among the more common reasons for referral to a breast clinic. They may be detected incidentally on screening mammography or patients may present with symptoms and signs such as mastalgia, nipple discharge, or a palpable mass.

Cystic breast disease has been recognized as the most frequent benign breast lesion in women. Up to one-third of women aged 30–50 years have cysts in their breasts. The true frequency is probably much greater than the clinically recognized entity, and the prevalence has been estimated to be between 50 and 90% (Chun et al., 2005; Mannello et al., 2006).

This study included 60 patients with the diagnosis of cystic breast lesions. In the current study, the youngest patient was 17 years and the oldest was 64 years, with mean age of 35±12 years. Taşkin et al., 2010 found an average age of 45±8 years among 60 women who had breast cyst. Shafqat et al., 2008 found that breast cysts were common in women older than 40 years. Tez et al., 2008 found that the mean age of patients who had a breast cyst was 47 years.

On analysis in the present study, it was found that all simple cysts were benign, most of the complicated cysts were benign, whereas four of 10 complex cysts in this study were malignant. Venta et al., 1999 found that 0.3% of 308 complicated cystic lesions in their study proved to be malignant. Buchberger et al., 1999 found that none of the 133 complicated cystic lesions in their study were malignant. Kolb et al., 1998 found that none of the 126 complicated cystic lesions in their study were malignant. Chang et al., 2007 found that seven of 27 complex cystic lesions in their study proved to be malignant. Taşkin et al., 2010 found that of 22 complex cysts with a solid component, five were malignant. He also found that the risk of malignancy among complicated cysts was less than 2%.

This study showed that most of the simple cysts had an acellular aspirate, whereas all complicated and complex cysts had a cellular aspirate fluid. Tez et al., 2008 found that insufficient cellular material was seen on examination of the aspirate fluid from 17 (10.3%) cysts and atypical cells were seen in four (2.4%) cysts.

The present study showed that there was no significant correlation between the cyst margin and the cytological study. Louie et al., 2003 found that breast cysts with irregular borders were evaluated as complicated cysts. Taşkin et al., 2010 found that 39 of 61 cysts with a thick cyst wall were complex cysts. Tez et al., 2008 found that all lesions with irregular borders were evaluated as complicated cysts.

This study showed that all complex and complicated cysts had enlarged axillary lymph nodes. There were no studies discussing the correlation between lymph node affection and different pathologies of breast cysts.

The present work showed that two thirds of the malignant cysts had thick septations, whereas cysts of benign pathologies (fibrocystic disease, abscess, hematomas) had either thin septations or none. Berg et al., 2003 found that 35% of the cystic masses with septa were malignant. Chang et al., 2007 found that 50% of the cysts with thick septations proved malignant. In contrast to this study, they found that abscesses and hematomas can also present as thick-wall cysts. Bassett, 2000 found that thin septations in a breast cyst represent a benign finding.

This study showed that all malignant cases had residual masses after cyst aspiration. Chang et al., 2007 found that 50% of the cysts with residual masses proved to be malignant. Bhate et al., 2007 found that all residual lumps and recurrent cysts are known to be associated with intracystic cancers.

The present study showed that 12 cysts of 60 cases that yielded a bloody aspirate had RBCs, with one cyst having malignant cells on cytology. Tez et al., 2008 stated that neither a bloody aspirate nor refilling of a complicated cyst is diagnostic of the underlying malignancy. Venta et al., 1999 found that 8% of all aspirated complicated cysts were bloody. In this study, it was found that the 24 cysts that yielded a yellowish aspirate were of benign pathologies. Ciatto et al., 1987 found that a cloudy yellowish aspirate fluid is typical of a benign cyst pathology.

In this study, it was found that the most prevalent pathology was fibrocystic disease, which was present in 47.6% of the cases, abscess was present in 20% of the cases, and malignant cysts were present in 10% of the cases. Pradhan and Dhakal, 2008 found that fibrocystic diseases occurred in 49% of the cases, abscess was present in 24% of the cases, whereas malignant lesions were present in 10% of the cases. Kumar, 2010 found that fibrocystic diseases were present in 41% of the cases, abscess was present in 22.6%, and neoplastic lesions in 7.4% of the cases.

Back to Top | Article Outline

Conclusion

From the current study, it is concluded that the accuracy of breast sonography combined with fine-needle aspiration in detecting and allowing the correct diagnosis of cysts is almost 100%. The use of sonography has reduced the number of biopsies performed for benign breast cysts significantly. Aspiration should be followed by excisional biopsy when (a) blood is aspirated or (b) when the mass does not completely disappear.

Back to Top | Article Outline

Acknowledgements

Conflicts of interest

There are no conflicts of interest.

Back to Top | Article Outline

References

Bassett LW (2000). Imaging of breast masses. Radiol Clin North Am 38:669–691.
Berg WA, Campassi CI, Ioffe OB (2003). Cystic lesions of the breast: sonographic-pathologic correlation. Radiology 227:183–191.
Bhate RD, Chakravorty A, Ebbs SR (2007). Management of breast cysts revisited. Int J Clin Pract 61:195–199.
Buchberger W, deKoekkoek-Doll P, Springer P, Obrist P, Dünser M (1999). Incidental findings on sonography of the breast: clinical significance and diagnostic workup. Am J Roentgenol 173:921–927.
Cardenosa GC (2007). Clinical breast imaging: a patient-focused teaching file Philadelphia: Lippincott Williams & Wilkins; 2007.
Chang YW, Kwon KH, Goo DE, Choi DL, Lee HK, Yang SB (2007). Sonographic differentiation of benign and malignant cystic lesions of the breast. J Ultrasound Med 26:47–53.
Chun J, Joseph KA, El-Tamer M, Rundle A, Jacobson J, Schnabel F (2005). Cohort study of women at risk for breast cancer and gross cystic disease. Am J Surg 190:583–587.
Ciatto S, Cariaggi P, Bulgaresi P (1987). The value of routine cytologic examination of breast cyst fluids. Acta Cytol 31:301–304.
Dennison G, Anand R, Makar SH, Pain JA (2003). A prospective study of the use of fine-needle aspiration cytology and core biopsy in the diagnosis of breast cancer. Breast J 9:491–493.
Enriori CL, Novelli JE, Cremona Mdel C, Hirsig RJ, Enriori PJ (1992). Biochemical study of cyst fluid in human breast cystic disease: a review. Breast Cancer Res Treat 24:1–9.
Gao L, Zhang MH, MH Zhu (2005). Histopathology and fine needle aspiratory cytology of 281 cases of breast mass: a comparison analysis. Acad J Sec Mil Med Univ 26:825–826.
Kolb TM, Lichy J, Newhouse JH (1998). Occult cancer in women with dense breasts: detection with screening US – diagnostic yield and tumor characteristics. Radiology 207:191–199.
Kopans DB (2006). Breast imaging :3rd ed..Philadelphia: Lippincott Williams & Wilkins; 2006.
Kumar R (2010). A clinicopathologic study of breast lumps in Bhairahwa, Nepal. Asian Pac J Cancer Prev 11:855–858.
Lamb PM, Perry NM, Vinnicombe SJ, Wells CA (2000). Correlation between ultrasound characteristics, mammographic findings and histological grade in patients with invasive ductal carcinoma of the breast. Clin Radiol 55:40–44.
Lindholm KOrell SR, Sterrett GF, Whitaker D (2003) Breast. Fine needle aspiration cytology :4th ed..India: Churchill Livingstone; 2003, 165–226.
Lioe TF (2007). The role of fine needle aspiration cytology and needle core biopsy in the diagnosis and management of breast. Cancer Oncol News 1:8–12.
Louie L, Velez N, Earnest D, Staren ED (2003). Management of nonpalpable ultrasound-indeterminate breast lesions. Surgery 134:667–673discussion 673–674.
Mannello F, Tonti GA, Papa S (2006). Human gross cyst breast disease and cystic fluid: Bio-molecular, morphological, and clinical studies. Breast Cancer Res Treat 97:115–129.
Mendoza P, Lacambra M, Tan PH, Tse GM (2011). Fine needle aspiration cytology of the breast: the nonmalignant categories. Patholog Res Int 2011:547–580.
Pradhan M, Dhakal HP (2008). Study of breast lump of 2246 cases by fine needle aspiration. J Nepal Med Assoc 47:205–209.
Rinaldi P, Ierardi C, Costantini M, Magno S, Giuliani M, Belli P, Bonomo L (2010). Cystic breast lesions: sonographic findings and clinical management. J Ultrasound Med 29:1617–1626.
Sartorius OW (1995). The biochemistry of breast cyst fluids and duct secretions. Breast Cancer Res Treat 35:255–266.
Shafqat G, Iqbal F, Masroor I, Khanda G (2008). Sonographically diagnosed complex or complicated breast cyst with histopathological correlation to specifically address the need for intervention. PJR 18:33–36.
Stavros ATStavros AT (2004). Sonographic evaluation of breast cysts. Breast ultrasound Philadelphia: Lippincott Williams & Wilkins; 2004, 276–350.
Stavros AT, Thickman D, Rapp CL, Dennis MA, Parker SH, Sisney GA (1995). Solid breast nodules: use of sonography to distinguish between benign and malignant lesions. Radiology 196:123–134.
Taşkin F, Köseoğlu K, Özbaş S, Erkuş M, Karaman C (2010). Complex breast cysts: sonographic findings and histopathologic results. J Breast Health 6:135–140.
Tez S, Dener C, Köktener A, Caydere M, Tez M (2008). The value of fine needle aspiration and cytologic examination of impalpable complicated breast cysts. Bratisl Lek Listy 109:387–390.
Venta LA, Kim JP, Pelloski CE, Morrow M (1999). Management of complex breast cysts. Am J Roentgenol 173:1331–1336.
Yang IIY, Bao L (2000). Value of fine needle aspiration cytology in the diagnosis of breast cancer. Matern Child Health China 25:1995–1996.
Zakhour H, Wells C (1999). Diagnostic cytopathology of the breast London, UK: Churchill Livingstone; 1999.
©2014Egyptian Journal of Pathology