February 2013, VOLUME 200
NUMBER 2

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February 2013, Volume 200, Number 2

FOCUS ON: Women's Imaging

Clinical Perspective

Breast Imaging of the Pregnant and Lactating Patient: Physiologic Changes and Common Benign Entities

+ Affiliations:
1 Department of Diagnostic Imaging, Yale University School of Medicine, New Haven, CT.

2 Present address: Synergy Radiology Associates, PA, 7026 Old Katy Rd, Ste 276, Houston, TX 77024.

Citation: American Journal of Roentgenology. 2013;200: 329-336. 10.2214/AJR.12.9845

ABSTRACT
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OBJECTIVE. The purpose of this article is to review key clinical, histologic, and imaging features of expected physiologic changes within the breast and common benign breast disease in the pregnant and lactating patient.

CONCLUSION. A thorough understanding of expected physiologic changes and common benign breast abnormalities of pregnancy and lactation is required to differentiate these entities from pregnancy-associated breast cancer and to appropriately guide patient management.

Keywords: breast imaging, lactation, pregnancy, pregnancy-associated breast cancer

The presentation of a pregnant or lactating woman with a palpable breast mass is a scenario commonly encountered in many breast imaging practices. The unique physiologic changes that occur within the breast secondary to the hormonal changes of pregnancy and lactation result in increased breast volume and increased water content, with associated palpable nodularity, firmness, and increased parenchymal density. These changes may make clinical and radiologic evaluations of the breast difficult.

Eighty percent of patients presenting with a palpable breast mass during pregnancy and lactation will have findings of benign disease [13]. Successful management of these patients requires an understanding of expected clinical and imaging findings associated with physiologic breast changes and with common benign breast disease.

Physiologic Changes of Pregnancy and Lactation
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Alterations in circulating serum estrogen, progesterone, and prolactin levels are primarily responsible for the major physiologic changes during pregnancy and lactation. Beginning in the first trimester and continuing throughout pregnancy, increasing estrogen levels stimulate growth of the breasts predominantly through the development and arborization of the ductal system and, to a lesser extent, through increasing stromal adipose tissue [4, 5]. Progesterone acts synergistically with estrogen to contribute to ductal and lobular growth and is responsible for providing secretory capability to alveolar cells, which is required for milk synthesis [4].

Despite the integral role of estrogen and progesterone in preparation for lactation, both inhibit milk production. Colostrum is secreted into the ductal system in the final days of pregnancy but at the rate of only a few milliliters per day [4]. Milk production at full capacity begins after childbirth when the stimulatory effects of prolactin act un-opposed by the inhibitory effects of placental estrogen and progesterone [4, 5]. Secretion of prolactin from the pituitary gland steadily increases throughout pregnancy but returns to basal levels postpartum [4]. Milk synthesis is sustained by each breast-feeding event, which stimulates biofeedback resulting in high-level intermittent prolactin secretion.

Physiologic changes manifest clinically with increased breast size, firmness, and nodularity, which make the physical examination progressively more difficult as pregnancy advances. These findings are maintained during lactation and will steadily progress back to the prepreg-nancy state approximately 3 months after cessation of breast-feeding. Therefore, a thorough baseline clinical breast examination at the first obstetric visit is recommended [6].

Changes in breast physiology correlate with histologic changes seen in the progression from the prepregnancy to postlactation state (Fig. 1). Although the histologic appearance of normal breast parenchyma varies with the menstrual cycle, lumina are generally collapsed with the exception of minimal secretions in the luteal phase [5]. At the alveolar level, during the first trimester of pregnancy the two-layer epithelial structure of the prepregnancy state is maintained. During the second and third trimesters the superficial layer differentiates into a colostrum cell layer with associated eosinophilic cells, plasma cells, and leukocytes [5]. Throughout pregnancy there is progressive enlargement of the lobules with increasing luminal distention in the second and third trimesters. Luminal distention is most marked during lactation and will regress with shrinking lobules in the postlactation period.

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Fig. 1A —Photomicrographs (H and E; ×40).

A, Normal breast tissue in 25-year-old woman who is not pregnant shows lobules with collapsed lumina, dense stroma, and mononuclear infiltrate.

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Fig. 1B —Photomicrographs (H and E; ×40).

B, Normal breast tissue in 33-year-old pregnant woman shows extensive lactational changes. During pregnancy, lobules increase at expense of interlobular adipose tissue. Lumina are open with eosinophilic secretions.

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Fig. 1C —Photomicrographs (H and E; ×40).

C, Normal breast tissue in 29-year-old woman 2 weeks postpartum shows lobules markedly distended with secretions and vacuolated cytoplasm in epithelial cells.

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Fig. 1D —Photomicrographs (H and E; ×40).

D, Normal breast tissue in 27-year-old woman after cessation of breast-feeding shows lobules have begun to shrink; mononuclear infiltrate is commonly found in intralobular stroma.

Several physiologic changes of pregnancy and lactation show imaging correlates on ultrasound examination. Lobular growth is reflected by increased echogenicity of normal breast parenchyma throughout pregnancy. In the final days of pregnancy, tubular hypoechoic structures are seen, representing colostrumfilled ducts (Fig. 2). Colostrum differs from postpartum breast milk in that it contains almost no fat [4], thus explaining its hypoechoic appearance on ultrasound. During lactation, most breast parenchyma appears echogenic, resulting from the combination of glandular enlargement and engorgement of breast tissue with milk rich in fat. In both pregnancy and lactation, hypervascularity of the breast tissue can be observed [7] (Fig. 3). After cessation of breast-feeding, the sonographic appearance of the breast returns to the prepregnancy state.

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Fig. 2 —30-year-old woman, 40 weeks pregnant, with bloody nipple discharge. Gray-scale ultrasound image shows prominent hypoechoic ducts filled with colostrum and no underlying mass. Because colostrum contains very little fat, ductal secretions are hypoechoic.

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Fig. 3A —37-year-old lactating woman with palpable breast mass.

A, Gray-scale ultrasound image shows markedly echogenic breast tissue and no underlying mass. These findings are normal in lactating patients and are due to engorged, milk-filled breasts.

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Fig. 3B —37-year-old lactating woman with palpable breast mass.

B, Color Doppler ultrasound image shows generalized hypervascularity, also normal in lactating patients.

The primary mammographic manifestation of the physiologic changes of pregnancy and lactation is increased breast size and density. These changes may be most pronounced during early lactation and the late third trimester (Fig. 4). It may be helpful to ask the lactating patient to nurse or pump before mammography to decrease the density of the engorged breast.

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Fig. 4A —Bilateral mammograms of 36-year-old breast-feeding woman.

A, Image show breasts are extremely dense.

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Fig. 4B —Bilateral mammograms of 36-year-old breast-feeding woman.

B, Image show breasts are extremely dense.

MRI performed during lactation will also reflect expected physiologic changes. A case report of a lactating patient without breast cancer and a case series of seven lactating patients, five of whom had biopsy-proven breast cancer, described MRI findings of increased background enhancement and of diffusely increased T2 signal in lactating patients [8, 9]. Increased and rapid diffuse breast enhancement has been attributed to the increased vascularity of the lactating breast, and the diffuse increased T2 signal is thought to be secondary to the aqueous nature of breast milk.

Bloody Nipple Discharge
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Bloody nipple discharge is occasionally encountered during pregnancy, usually during the third trimester [10], and is most often benign. A proposed cause of bloody nipple discharge includes unnoticed minimal breast trauma in the setting of epithelial proliferation and new capillary formation [11]. Although blood in nipple discharge may not always be clinically apparent, cytologic analysis showed RBCs were present in 20% of women with nipple discharge during pregnancy and 23% of lactating women [10, 12, 13]. Bloody nipple discharge without an associated mass is rarely seen as a presenting symptom of pregnancy-associated breast cancer [10, 14].

In cases of spontaneous, unilateral bloody nipple discharge in the absence of a palpable mass, ultrasound can be performed to evaluate the retroareolar ducts to exclude a papilloma or intraductal carcinoma [11]. Ductography can also be safely performed and can be considered if cytologic findings are suspicious and discharge originates from a single duct [10, 11]. Postpartum contrast-enhanced MRI may also be useful for further workup in selected cases if clinically indicated [15, 16].

Fibroadenoma
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The most common benign tumor detected during pregnancy and lactation is a fibroadenoma [11]. Fibroadenomas are usually present before pregnancy but may not be clinically apparent until they grow under the influence of hormonal stimuli [5] and present as a “new” or enlarging palpable mass. Fibroadenomas typically present as painless firm, mobile, and rubbery masses. Fibroadenomas may occasionally become infarcted secondary to rapid growth outpacing the vascular supply. Infarcted fibroadenomas may differ from typical fibroadenomas and present as tender nonmobile masses [7].

Fibroadenomas arise in the terminal ductal lobular unit and contain both epithelial and stromal components [5, 7]. The epithelial component consists of glandlike ductal spaces, and the stromal component is made up of connective tissue [5]. Hyalinization, calcification, and ossification of the stromal elements may be seen in older lesions in postmenopausal patients but are atypical in lesions found in the pregnant and lactating patient [5]. Fibroadenomas in pregnant and lactating patients occasionally show secretory hyperplasia or lactational change on histologic examination but are generally considered to be distinct from lactating adenomas.

The most common sonographic appearance of fibroadenomas in pregnant and lactating women is similar to that seen in nongestational patients: an oval or round mass with a wider-than-tall orientation, with a circumscribed margin, and with or without a few gentle lobulations [5] (Fig. 5). Fibroadenomas are often multiple and bilateral. Ultrasound-guided biopsy should be considered for any new solid mass in a pregnant or lactating patient despite a benign ultrasound appearance. Infarcted fibroadenomas may show internal cystic spaces and a more irregular border than typical fibroadenomas [7], and these suspicious features should prompt biopsy (Fig. 6). In nonpregnant patients, biopsy-proven fibroadenomas with slight growth of up to 20% may be safely followed with a 6-month follow-up ultrasound examination and may not require rebiopsy [17]. The same criteria may also be applied to documented preexisting fibroadenomas that show growth during pregnancy, but meticulous scanning is necessary to exclude suspicious features (Fig. 7).

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Fig. 5 —37-year-old woman, 7 weeks pregnant, with new palpable right breast mass that was noted to be simple cyst on ultrasound image not adjacent to this solid well-circumscribed incidentally seen oval hypoechoic mass, consistent with fibroadenoma. Although this mass was not biopsied; short-interval ultrasound follow-up was advised because of benign ultrasound features and patient's history of two prior palpable biopsy-proven right breast fibroadenomas.

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Fig. 6A —28-year-old pregnant woman in first trimester of first pregnancy with rapidly enlarging 7-cm palpable breast mass.

A, Targeted gray-scale ultrasound image shows oval circumscribed heterogeneous mass with small cystic components.

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Fig. 6B —28-year-old pregnant woman in first trimester of first pregnancy with rapidly enlarging 7-cm palpable breast mass.

B, Color Doppler ultrasound image shows internal and predominately peripheral vascularity. These findings are consistent with infarcting fibroadenoma, but malignancy cannot be excluded. Ultrasound-guided core needle biopsy showed fibroadenoma without infarction. Lack of infarction was likely secondary to undersampling.

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Fig. 7 —29-year-old woman, 32 weeks pregnant, referred for short-interval follow-up of palpable biopsy-proven fibroadenoma in left breast. Gray-scale ultrasound image shows oval predominately echogenic mass with indistinct margins. Mass had also increased from 1.9 × 1.1 × 1.9 cm to 2.7 × 1.7 × 2.5 cm. Because this increase is greater than 20% and margins was not circumscribed, surgical excisional biopsy was performed; results confirmed diagnosis of fibroadenoma.

Lactating Adenoma
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Lactating adenomas are seen primarily during lactation and the third trimester of pregnancy but may occasionally be observed in the first and second trimesters of pregnancy [5, 7]. Lactating adenomas present very similarly to fibroadenomas as painless, soft, mobile masses [7]. They may also become infarcted and present atypically as a firm tender mass. A un ique feature of lactating adenomas is the tendency to regress after cessation of breast-feeding [18].

Lactating adenomas differ histologically from fibroadenomas in that they consistent predominantly of epithelial elements with a very minimal stromal component [5]. The epithelial component consists of mature tubules similar to those found in normal lobules. The tubules contain actively secreting cells resulting in acini distended with secretions [7].

A lactating adenoma may be indistinguishable from a fibroadenoma on sonography (Fig. 8). Like fibroadenomas, lactating adenomas may be multiple and bilateral. Lactating adenomas typically appear as oval masses with a wider-than-tall orientation, posterior acoustic enhancement, and a circumscribed margin [7, 18]. A microlobulated margin is often seen; investigators have postulated that each microlobulation represents an acinus distended with secretions [7]. The posterior acoustic enhancement is presumably secondary to the large amount of secretions. Increased lesion compressibility may be observed, perhaps for the same reason, on application of ultrasound probe pressure [7]. Infarcted lactating adenomas often show atypical features including posterior acoustic shadowing and irregular margins and are thus indistinguishable from other benign and malignant entities [7, 18] (Fig. 9).

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Fig. 8 —37-year-old woman, 37 weeks pregnant, with palpable right breast mass. Targeted gray-scale ultrasound image shows oval well-circumscribed hypoechoic mass; these features are characteristic of fibroadenoma. Mass proved to be lactating adenoma on ultrasound-guided core needle biopsy.

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Fig. 9A —23-year-old pregnant woman who presented during third trimester with bilateral painful palpable masses.

A, Gray-scale ultrasound image shows large (> 5 cm) oval heterogeneous hypoechoic mass in right upper outer quadrant.

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Fig. 9B —23-year-old pregnant woman who presented during third trimester with bilateral painful palpable masses.

B, Ultrasound image of left breast shows heterogeneous predominately hypoechoic mass that is more irregularly shaped than but otherwise similar to mass shown in A. Although these findings may be seen with infarction, malignancy cannot be excluded. Ultrasound-guided core needle biopsy confirmed bilateral lactating adenomas.

Galactocele
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A galactocele is the most common benign breast mass in the lactating patient [11]. Galactoceles are most often seen after cessation of breast-feeding but can also be seen during lactation and occasionally in the third trimester of pregnancy [7]. Galactoceles most commonly present as a painless palpable mass in the weeks or months after cessation of breast-feeding [7]. In cases that present during lactation, investigators have observed that the patient provides a history of decreased frequency of nursing [7].

Galactoceles occur as a result of obstruction of a duct and inspissation of milk [11]. Histologically, the lesion represents milk-dis-tended terminal ducts or ductules with normal associated epithelium and myoepithelium [5]. Galactoceles contain varying amounts of water, protein, fat, and lactose. Enzymes may denature the milk over time, resulting in coalescence of emulsified lipid droplets into larger globules [7].

The sonographic appearance of galactoceles is correspondingly variable and depends on fat content and lesion age (Fig. 10). Galactoceles are usually round or oval; may be anechoic, hypoechoic, or echogenic; and may show wall thickening in cases of chronic inflammation [19]. Galactoceles usually show increasing internal echogenicity as the lesion ages, and a fatfluid level is occasionally observed [7]. Even in cases with internal complex echoes, vascular flow should never be present; however, hyper-emia may be seen in the adjacent compressed breast parenchyma [7].

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Fig. 10A —Multiple galactoceles with variable appearances on gray-scale ultrasound images.

A, 28-year-old breast-feeding woman who presented with painful new mass in left breast. Targeted ultrasound image shows lobulated predominately anechoic galactocele with high water content and small amount of echogenic fat (arrow).

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Fig. 10B —Multiple galactoceles with variable appearances on gray-scale ultrasound images.

B, 31-year-old woman, 3 months postpartum, with new palpable right breast mass. Targeted ultrasound image shows predominately echogenic mass with fat-fluid level consistent with galactocele with high fat content.

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Fig. 10C —Multiple galactoceles with variable appearances on gray-scale ultrasound images.

C, 33-year-old breast-feeding woman with anechoic galactocele with high water content and subtle fat-fluid level (arrow).

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Fig. 10D —Multiple galactoceles with variable appearances on gray-scale ultrasound images.

D, 28-year-old breast-feeding woman with recurrent painful mass 3 weeks after aspiration of galactocele. Ultrasound shows complex mixed echogenicity oval mass with thick wall, consistent with recurrent galactocele. Ultrasound-guided biopsy revealed lactational breast tissue with acute and chronic inflammatory changes.

Most galactoceles will regress spontaneously and will not require aspiration. However, a galactocele may have a sonographic appearance of a complex mass or may be bothersome to the patient. In these cases, ultrasound-guided aspiration can be performed and will yield milky fluid (Fig. 10). Galactoceles may recur after aspiration and may also occasionally become superinfected; in these cases, aspiration may be diagnostic and therapeutic [5].

Mastitis
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Mastitis with or without abscess formation is commonly seen during lactation and is less frequently seen during pregnancy [5, 11]. The proposed cause of mastitis is retrograde infection through cracked nipples and poor emptying of milk [5]. The highest incidence of lactation-related mastitis is during the 6 weeks immediately postpartum, and the most likely infectious agents are Staphylococcus and Streptococcus bacteria [5, 20].

Clinically, patients may present with an edematous, erythematous, and tender breast [5, 7]. Uncomplicated mastitis is a clinical diagnosis that does not necessitate an imaging work-up. The presence of a fluctuant mass should raise suspicion of an underlying abscess [5].

Ultrasound should be performed if response to antibiotic therapy is poor or if abscess formation is suspected. Sonographic findings in early mastitis may be limited to regional edema and skin thickening [7]. As tissue necrosis begins in focal mastitis, skin thickening may be accompanied by a focal hypoechoic mass with surrounding hyperemia. In cases of focal mastitis, a focal inflammatory mass may occur and mimic the appearance of a solid mass. Careful clinical and ultrasound evaluation and follow-up are necessary to ensure proper diagnosis (Fig. 11). The sonographic features of a mature abscess are typically a thick-walled mass and posterior acoustic enhancement with or without internal gas and debris (Figs. 12 and 13).

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Fig. 11 —37-year-old lactating woman with focally painful, palpable left breast mass. Gray-scale ultrasound image shows irregular heterogeneous mass with mixed echogenicity and indistinct margins (arrow). Diagnosis of focal mastitis was made, biopsy was not performed, and antibiotic therapy was instituted. Follow-up ultrasound performed 1 week after completion of antibiotics (not shown) showed resolution of mass.

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Fig. 12A —37-year-old woman, 1 month postpartum and breast-feeding, who presented with left breast pain, palpable mass, and fever.

A, Skin thickening and edematous hypervascular breast on color Doppler ultrasound as shown are consistent with mastitis.

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Fig. 12B —37-year-old woman, 1 month postpartum and breast-feeding, who presented with left breast pain, palpable mass, and fever.

B, Palpable lump corresponded to this complex cystic mass on ultrasound, which is consistent with breast abscess.

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Fig. 12C —37-year-old woman, 1 month postpartum and breast-feeding, who presented with left breast pain, palpable mass, and fever.

C, Thirty-five milliliters of thick fluid was aspirated under ultrasound guidance using 18-gauge needle. Patient was treated with antibiotics.

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Fig. 13A —18-year-old pregnant woman with right breast erythema and induration.

A, Ultrasound image shows complex cystic mass. Note echogenic air with dirty shadowing (arrow) within mass.

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Fig. 13B —18-year-old pregnant woman with right breast erythema and induration.

B, Color Doppler ultrasound image shows marked peripheral hypervascularity. These findings are consistent with abscess.

Ultrasound-guided aspiration should be considered if an abscess is present to provide pain relief and to shorten illness duration [5, 7]. If the abscess persists or recurs, repeat aspiration should be performed for the same reasons [21]. Treatment also includes antibiotic therapy and pain management [20, 22]. If an underlying mass is suspected, core needle biopsy should also be performed [11, 20]. Patients can continue breast-feeding after the biopsy procedure, and it may be helpful to reduce milk stasis and the likelihood of recurrent abscess [20]. Clinical follow-up to ensure resolution is required in all patients. In atypical or refractory cases, further imaging with follow-up ultrasound and mammography should be considered [23]. In these cases, the decision to perform imaging-guided core needle biopsy or skin punch biopsy should be based on the presence of suspicious imaging or clinical features.

Conclusions
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Similar to nongestational patients, most pregnant and lactating patients presenting for breast imaging are found to have benign disease. However, all palpable masses in a pregnant or lactating patient that persist for 2 weeks or longer should be promptly evaluated with ultrasound. Biopsy should be considered for any new solid mass identified despite a benign appearance. If biopsy is not performed, then close imaging and clinical follow-up is necessary. A thorough understanding of the clinical and imaging features of normal physiologic changes and of common benign entities is required to differentiate these entities from pregnancy-associated breast cancer.

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Address correspondence to R. Vashi ().

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