Palpable masses in breast during lactation

Clinical Imaging 31 (2007) 1 – 5

Palpable masses in breast during lactation Silvia Obenauer4, Stephan Dammert Department of Radiology, Georg-August-University of Goettingen, 37 075 Go¨ttingen, Germany Received 5 July 2006; accepted 2 October 2006

Abstract Objectives: Diagnosis of breast cancer is more difficult in pregnant and lactating women. In the present study, the value of different radiological methods has been evaluated. Material and Methods: Twenty-seven patients with palpable breast masses during the lactation period were evaluated. All masses were investigated in the clinical course as well as in ultrasound. If ultrasound demonstrated a suspicious lesion a mammogram was done. If clinical course, ultrasound, and mammography could not rule out breast cancer, MR mammography was done. Results: Eighteen ultrasound-guided biopsies were done, revealing three cysts, seven hyperplasias/mastopathia, three cases of papilloma, and two carcinomas. The 18 mammograms were classified as BI-RADS 1 and 2 in nine cases, as BI-RADS 3 in seven cases, as BI-RADS 4 in one case, and as BI-RADS 5 in also one case. MR mammography was done in 9 cases revealing three BI-RADS 4 categories and one BI-RADS 5 category, all of them showed a malignant histology. Conclusions: The density of the lactating breast compromises breast cancer diagnosis. Ultrasound should be the method of choice. If possible mammography and MR mammography should be done after lactating period. D 2007 Elsevier Inc. All rights reserved. Keywords: Lactating period; Ultrasound; Mammography; MR mammography

1. Introduction The incidence of breast cancer discovered during pregnancy or lactation ranges from one case per 1300 pregnancies to one case per 6200 pregnancies [1]. Since an increasing number of women are electing to postpone pregnancy to their late thirties and forties, the incidence of breast cancer concurrent with pregnancy is increasing. This clinical situation is particularly devastating because the diagnosis is frequently delayed and made when the cancer stage has progressed because of difficulties in clinical breast examination during pregnancy and the lactation period. The patient is appropriately depressed and loses confidence in her physicians [2]. The psychosocial consequences for the family are profound. Furthermore, diagnosis of breast cancer is more difficult in pregnant and lactating women. It has been stated that pregnant and lactating women have extremely dense breasts secondary to increased vascularity, 4 Corresponding author. Tel.: +49 0551/398965; fax: +49 0551/399606. E-mail address: [email protected] (S. Obenauer). 0899-7071/07/$ – see front matter D 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.clinimag.2006.10.005

glandular tissue, and the presence of milk and that this increased density compromises the ability to identify disease in the clinical course and at mammography [3]. Furthermore, no published literature on the normal gestational breast appearance aids in the ultrasonographic diagnosis of a questionable mass on physical examination [4]. The advantage of contrast-enhanced magnetic resonance (MR) imaging of the breast is its high sensitivity to invasive breast cancer; however, MR mammography is also limited in pregnant and lactating women [5 –16]. In the present retrospective study, the value of the different radiological methods in lactating women has been evaluated. 2. Materials and methods The study group included 27 patients (age: range, 25 – 41 years; mean, 33 years) with palpable breast masses during the lactation period. All masses were investigated in the clinical course (inspection and palpation) as well as in ultrasound with a high-resolution system (Logic 400CL, General Electric, Milwaukee, WI, USA). If palpation or ultrasound

2

S. Obenauer, S. Dammert / Clinical Imaging 31 (2007) 1 – 5

Table 1 Twenty-seven patients in lactating period with suspicion of palpable mass Mammography Patient

Age (years)

Palpable mass

Ultrasound

ACR

BI-RADS

MR mammography

Procedure

Histology

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

33 32 33 35 33 32 41 35 31 33 25 33 28 30 29 29 29 30 29 30 27 39 38 27 36 33 36

L(2) R L L L L R R R L L R L R L L R R R L – – R L R L R

5 3 3 4 2 3 3 2 3 3 3 2 2 2 2 3 3 1 2 1 2 2 2 2 2 2 2

2 3 4 3 2 4 4 – 3 4 3 4 – 2 – 3 3 – – 3 – – 3 – 4 – 3

5 3 4 3 3 3 1 – 1 2 3 2 – 3 – 3 1 – – 1 – – 1 – 2 – 1

I 4; II 4 5 4 4 3 1 1 1 2 – – – – – – – – – – – – – – – – – –

Surgery FNA+Surgery FNA+Surgery Surgery Biopsy FNA Biopsy Follow-up Biopsy FNA FNA FNA FNA FNA FNA FNA FNA Follow-up FNA Follow-up Follow-up Follow-up Follow-up FNA FNA FNA Follow-up

Bifocal IDC IDC IDC (G3) IDC (G2) Papilloma Hyperplasia Mastopathia – Parenchyma Mastitis Mastitis Mastitis Fibroadenoma Fibroadenoma Hyperplasia Hyperplasia Hyperplasia – Parenchyma – – – – Cyst Cyst Milk cyst –

Classification of suspicious lesions in ultrasound, mammography, and MR mammography, according to BI-RADS. Correlation with cytology, histology, or follow-up.

was negative or if ultrasound revealed a benign lesion (e.g., cyst), no further diagnostic evaluation was necessary. If ultrasound demonstrated a suspicious lesion, a mammogram in oblique view was done at the digital mammography system Senographe 2000D (General Electric). If clinical course, ultrasound, and mammography could not rule out breast cancer, MR mammography was done, which was also necessary for staging breast cancer preoperatively (size of tumor, multifocality, multicentricity, contralateral tumor, and intraductal tumor component).

Breast MR imaging was performed with a 1.5-T system (Magnetom Vision, Siemens, Erlangen, Germany) by using a dedicated bilateral breast surface coil in combination with a prototype compression device [9]. A two-dimensional fast low angle shot (2D-FLASH) pulse sequence with a repetition time (TR) of 375 ms, an echo time (TE) of 5 ms, and a flip angle (FA) of 908 was used. The sequence yielded thirty-two 4-mm-thick transverse slices (matrix, 210256) without gaps in an acquisition time of 81 s. The entire breast was imaged before and five times after

Table 2 Criterion in MR mammography according to the Goettinger score system of the patients who underwent MR mammography in the lactating period Morphology

Dynamics

Number

Form

Contour

Enhancement

Initial SI

Postinitial SI

Score

1

Polygonal Polygonal Spiculated Polygonal Polygonal Dendritic No lesion Polygonal No lesion Linear

Unsharp Sharp Unsharp Unsharp Unsharp Sharp

Rim Rim Rim Inhomogenous Rim Homogenous

N100% 50–100% N100% N100% 50–100% 50–100%

Plateau Wash-out Plateau Plateau Plateau Plateau

Sharp

Homogenous

50–100%

Continuous

Sharp

Homogenous

50–100%

Continuous

6 5 7 5 5 3 0 1 0 2

2 3 4 5 6 7 8 9

S. Obenauer, S. Dammert / Clinical Imaging 31 (2007) 1 – 5

3

phase (increase, plateau, or wash out) were taken into consideration according to the Goettinger score. Ultrasound and mammograms were classified in accordance to the breast imaging reporting and data system (BI-RADS) categories. In MR mammography, form and contour of the lesions were evaluated, and the dynamics of contrast enhancement (initial signal intensity and postinitial signal intensity) were measured [9,17]. In 20 cases, clinical and radiological results could be correlated with cytology or histology. The remainder cases were evaluated in the follow-up.

3. Results Fig. 1. Mammography shows a cluster of suspicious microcalcifications. Histology confirmed IDC.

intravenous administration of 0.1 mmol of gadopentetate dimeglumine (Magnevist, Schering, Berlin, Germany) per kilogram of body weight without time gaps. Postprocessing included subtraction of the unenhanced images from the contrast-enhanced images on a pixel-to-pixel basis, calculation of the time–intensity curve of any lesion, and a maximum intensity projection reconstruction (MIP). The ROI was placed within the area of the most intense enhancement. The enhancement amplitude was calculated as percentage of the precontrast signal intensity:

Time between birth of the child and appearance of palpable mass varied between 1 week and 12 months. Five patients suffered of risk factors for breast cancer.

ðSIpost  SIpreÞ= SIpre  100% where SI post indicates postcontrast signal intensity and SI pre indicates precontrast signal intensity. For signal time curve evaluation, the steepness of the initial enhancement and the characteristics of the postinitial

Fig. 2. MR mammography reveals no suspicious lesion in T1-weighted imaging. After contrast media application, subtraction image shows diffuse enhancement without suspicious lesion in MR mammography.

Fig. 3. In mammography, a BI-RADS-5-classified lesion was found on the left side. MR mammography confirmed the suspicious lesion. Furthermore, a second lesion with suspicious contrast media enhancement was diagnosed. Histology revealed bifocal IDC.

4

S. Obenauer, S. Dammert / Clinical Imaging 31 (2007) 1 – 5

In 25 of 27 patients, the palpable mass could be confirmed by the physician. In the remainder two patients, no palpable mass was confirmed. Ultrasound of the two patients without palpable mass revealed an asymptomatic cyst with no change in the follow-up. In three cases, ultrasound demonstrated a cyst at the location of the palpable mass, which was punctuated in two cases, revealing no malignancy. In a further patient, cytology revealed a milk cyst. In one case, ultrasound showed without doubt a galactocele, which disappeared after 3 months follow-up in ultrasound. Three of these seven patients have had a mammography without any suspicious lesion. No further diagnostic imaging was necessary in these patients. In the remainder 20 patients, ultrasound showed a lesion suspected of malignancy with unclear border and pathological echotexture classified as BI-RADS 4 or 5 (n=2), a probably benign lesion classified as BI-RADS 3 (n=9), an asymmetric lesion (n=1) or a well-defined lesion with the criterion of benignity categorized as BI-RADS 2 (n=6), and no suspicious lesion (n=2). In 15 cases out of the 20 patients, mammography was done. In both patients with a highly suspicious lesion in ultrasound, bilateral mammography was done. The sonographically found lesions were classified in mammography as BI-RADS 3 in one case, and a further lesion suspected of malignancy was found in mammography in the other case; both lesions classified as BI-RADS 5. Through MR mammography, the lesion found in the first case was confirmed to have the histology of an invasive ductal carcinoma (IDC; pT2, N1, M0, G2), and the two lesions in the second case were confirmed to be hypervascularized lesions with the histology of an IDC (pT2, N1, M0, G2) (Tables 1 and 2). All the nine patients with BI-RADS-3-classified lesions in ultrasound got further diagnostic evaluation in mammography. Mammography revealed no suspicious or typical benign lesion in four cases; four lesions classified as BI-RADS 3, and one as BI-RADS 4 (microcalcifications). In five of these nine patients, MR mammography was done, revealing three cases without suspicious lesions and two cases classified as BI-RADS 4 or 5. In these two cases, fine-needle aspiration biopsy (FNA) confirmed malignancy, whereas FNA or biopsy in the other cases revealed benign histology. MR mammography was also done in two patients with typical benign ultrasound imaging. In one case, no suspicious lesion was found without malignancy in the clinical follow-up. In the other case, MR mammography confirmed a lesion classified as BI-RADS 3; biopsy revealed papilloma. Eighteen ultrasound-guided biopsies (15 FNA cytologies and 3 tru-cut biopsies) were done, revealing three cysts, seven hyperplasias/mastopathia, three cases of puerperal mastitis, two fibroadenomas, one case of papilloma, and two carcinomas. The 18 mammographies of the pregnant or lactating women showed a fibroglandular (n=3), dense (n=9), or extreme dense (n=6) breast tissue, according to the BI-RADS classification. The mammograms were classified as BI-RADS 1 and 2 in nine cases, as

BI-RADS 3 in seven cases, BI-RADS 4 in one case, and BI-RADS 5 in another case. MR mammography was done in nine cases (Figs. 1–3).

4. Discussion According to the literature, breast cancer occurred in pregnancy and lactation period in 0.2–3.8% of all breast diseases [4,6]. Petrek et al. (1991) reported a 15% incidence of pregnancy among breast cancer patients less than 40 years of age. However, the correlation between breast cancer and pregnancy/lactating period has been discussed controversially [18]. DiFronzo and O’Connell reported that pregnancy/lactating period and breast cancer are merely coincidental and do not, however, directly contribute to the development or accelerated progression of breast cancer [19]. The majority of studies have documented a significant delay in diagnosis secondary to physiologic changes of the breast during pregnancy/lactating period and have reasoned that this is the likely explanation for the advanced stage of the disease upon initial presentation. The majority of studies are consistent with the present findings that women with pregnancy- or lactating-associated breast cancer present with more advanced disease, especially in terms of lymph node status than do those who are not pregnant [18,20]. A number of possible explanations have been proposed, including delay of diagnosis, difficulties in tumor detection in those with breast engorgement and hypertrophy, and medical attention diverted to the pregnancy or lactating period rather than routine health checks. The diagnostic procedure in pregnant or lactating women with a palpable mass is very difficult due to a dense breast in which it is difficult to recognize individual structures and to define pathological processes. Ultrasound is of course an important tool in investigating patients in pregnancy or lactating period with a suspicious palpable mass. In ultrasound, a cyst and/or galactocele could be detected without doubt, resulting in no further diagnostic evaluation. Furthermore, when a suspicious lesion in ultrasound is revealed, ultrasoundguided FNA or biopsy would be the method of choice [1]. If a lactating patient has a palpable mass without pathology in ultrasound, mammography should be done to reveal microcalcifications. There are some case reports of microcalcifications occurring in lactation period without malignancy [21]. However, mammography before the age of 35 years should be done only in cases with suspicious palpable mass or risk factors for breast cancer [5,8,22–24]. The density of the lactating breast and diagnosis in mammography are discussed controversially in literature [2,3]. When mammography is done, it should be after lactation of the breast [4]. Low-exposure parameters and one-view mammograms using a digital system should be recommended. MR mammography shows limitation in the lactating period due to dense breast and consecutive high false-positives. Often there is high enhancement in the lactating period;

S. Obenauer, S. Dammert / Clinical Imaging 31 (2007) 1 – 5

however, in our study, MR mammography was not limited in eight of nine cases.

[12]

References [13] [1] Bottles K, Taylor R. Diagnosis of breast masses in pregnant and lactating women by aspiration cytology. Obstet Gynecol 1985;66: 76 – 8. [2] Kuerer M. Breast carcinoma associated with pregnancy and lactation. Surg Oncol 1997;6:93 – 8. [3] Swinford AE, Adler DD, Graver KA. Mammographic appearance of the breasts during pregnancy and lactation: false assumptions. Acad Radiol 1998;5:467 – 72. [4] Petrek JA. Breast cancer and pregnancy. In: Harris JR, Hellmann S, editors. Breast diseases. 2nd ed. Philadelphia7 Lippincott; 1987. pp. 809 – 16. [5] Treves N, Holleb AI. A report of 549 cases of breast cancer in women 35 years of age or younger. Surg Gynecol Obstet 1958; 107:271 – 83. [6] Applewhite RR, Smith LR, DeVicenti F. Carcinoma of the breast associated with pregnancy and lactation. Am Surg 1973; 39:101 – 4. [7] Wallack MK, Wolf JA, Bedwinek J, et al. Gestational carcinoma of the female breast. Curr Probl Cancer 1983;7:1 – 58. [8] Horsley JS, Alrich EM, Wright CB. Carcinoma of the breast in women 35 years of age and younger. Ann Surg 1969;169:839 – 43. [9] Fischer U, Kopka L, Grabbe E. Breast carcinoma: effect of preoperative contrast-enhanced MR-imaging on the therapeutic approach. Radiology 1999;213:881 – 8. [10] Heywang SH, Wolf A, Pruss E, Hilbertz T, Eiermann W, Permanetter W. MR imaging of the breast with Gd-DTPA: use and limitations. Radiology 1989;171:95 – 103. [11] Kuhl CK, Mielcareck P, Klaschik S, Leutner C, Wardelmann E, Gieseke J, Schild HH. Dynamic breast MR imaging: are signal

[14] [15]

[16] [17]

[18] [19] [20] [21]

[22]

[23] [24]

5

intensity time course data useful for differential diagnosis of enhancing lesions? Radiology 1999;211:101 – 10. Mqller-Schimpfle M, Ohmenh7user K, Stoll P, Dietz K, Claussen CD. Menstrual cycle and age: influence on parenchymal contrast medium enhancement in MR imaging of the breast. Radiology 1997;203:145 – 9. Kuhl CK, Bieling HB, Gieseke J, Kreft BP, Sommer T, Lutterbey G, Schild HH. Healthy premenopausal breast parenchyma in dynamic contrast-enhanced MR imaging of the breast: normal contrast medium enhancement and cyclical-phase dependency. Radiology 1997;203: 137 – 44. Kaiser WA. MR Mammography. Berlin7 Springer; 1993. Kaiser WA. False positive results in dynamic MR mammography Causes, frequency and methods to avoid. MRI Clin N Am 1994; 2:539 – 54. Nunes LW, Schnall MD, Orel SG, et al. Breast MR imaging interpretation model. Radiology 1997;202:833 – 41. American College of Radiology (ACR) SG. Illustrated breast imaging reporting and data system (BI-RADS). 3rd ed. Reston (Va)7 American College of Radiology; 1998. Petrek JA, Dukoff R, Rogatko A. Prognosis of pregnancy-associated breast cancer. Cancer 1991;67:869 – 72. DiFronzo L, O’Connell T. Breast cancer in pregnancy and lactation. Surg Clin North Am 1996;76:267 – 78. Ribeiro G, Palmer MK. Breast cancer associated with pregnancy A clinician’s dilemma. Br Med J 1977;2:1524 – 7. Stucker D, Ikeda D, Hartman A, Carlson R. New bilateral microcalcification at mammography in a postlactational woman: case report. Radiology 2000;217:247 – 50. Lethaby A, O’Neill M, Harvey V. Overall survival from breast cancer in women pregnant or lactating at or after diagnosis. Int J Cancer 1996;67:751 – 5. Liberman I, Giess C, Dershaw D, Petrek JA. Imaging of pregnancyassociated breast cancer. Radiology 1994;191:245 – 8. Schotte K, Cocquyt V, Dhondt M, VanBelle S. Breast cancer during pregnancy. Acta Clin Belg 2000;55:102 – 8.