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Morphological Changes in Breast Tissue with Menstrual Cycle Rathi Ramakrishnan, M.D

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Morphological Changes in Breast Tissue with Menstrual Cycle Rathi Ramakrishnan, M.D Morphological Changes in Breast Tissue with Menstrual Cycle Rathi Ramakrishnan, M.D. (Path.), Seema A. Khan, M.D., Sunil Badve, M.D., F.R.C.Path. Departments of Surgery (RR, SAK) and Pathology (SB), Northwestern University Medical School, Chicago, Illinois and Department of Pathology, Indiana University School of Medicine (SB), Indianapolis, Indiana retrospective analysis of large archival databases to Whether the breast tissue undergoes morphologic analyze the effect of timing of surgery in relation to changes in relation to the menstrual cycle had been menstrual cycle phase. It will also aid the design of a subject of debate. Elegant studies performed in epidemiological studies for breast cancer risk the early 1980s provided conclusive evidence of cy- assessment. clical changes in the normal breast lobules. These studies were almost entirely based on autopsy ma- KEY WORDS: Breast, Menstrual cycle classification, terial and have not been validated in the clinical Menstrual morphology. setting. In the present study, we examine breast Mod Pathol 2002;15(12):1348–1356 tissues from surgical specimens from 73 premeno- pausal women and use morphological criteria to The normal breast undergoes changes through the characterize the stage of the menstrual cycle. Pa- menstrual cycle that affect all aspects of breast tients taking oral contraceptives or hormonal ther- morphology, protein expression, and cell kinetics. apy were excluded from this study. The following This physiologic cycling appears to be disturbed in histological parameters were used to assess the women with breast cancer and may reflect a global menstrual stage: number of cell layers in the acini dysregulation of response to hormonal influences and presence and degree of vacuolation of the myo- epithelial cells, stromal edema, infiltrate, mitosis, (1, 2). These findings lend greater impetus to stud- and apoptosis. The morphological stage was then ies of normal breast physiology and its possible correlated with the stage of the cycle, as determined aberrations in women who are at increased risk for by last menstrual period and the usual menstrual cancer. There is a new urgency to this problem cycle length and in some patients with serum estro- because large, well-defined cohorts of women who gen and progesterone levels. The morphologic stage have undergone breast biopsy are now available, was concordant with dates in 54 of the 73 patients and the emergence of successful chemopreventive In 31 of these patients, serum levels options (3–5) has imparted a practical significance .(001. ؍ P ,74%) of estradiol and progesterone at the time of surgery to the task of identifying markers of risk and surro- were available for correlation. Twenty-five (80%) of gate markers of chemopreventive success in breast these were phase concordant by morphology and cells. The importance of morphological dating of -and 25 (80%), by dates breast in a clinical setting is 2-fold. One, the knowl ,(01. ؍ progesterone levels (P Women with a edge of the histological alterations occurring in the .(007. ؍ and progesterone levels (P high morphologic score were seven times as likely breast with the fluctuating hormonal milieu would to be in luteal phase as were women with a low enable the identification and enrollment of a cycle- score (odds ratio, 7.1; 95% confidence interval). matched subset in epidemiological studies relating Menstrual phase can be determined by the mor- to breast cancer risk. Two, some but not all studies phology of the normal lobules present within the have suggested an additional prognostic benefit for surgically excised breast specimens. This will permit patients if surgery is performed during the luteal half of the menstrual cycle. This issue can be reex- amined by retrospective morphologic dating of the Copyright © 2002 by The United States and Canadian Academy of Pathology, Inc. breast tissue relative to the menstrual cycle to ex- VOL. 15, NO. 12, P. 1348, 2002 Printed in the U.S.A. clude discrepancies associated with chronological Date of acceptance: September 6, 2002. Address reprint requests to: Sunil Badve, M.D., F.R.C.Path., Department of dating and anovulatory cycles (6–8). There is thus a Surgical Pathology, University Hospital, Room 3465, 550 North University need for a method for assessing breast samples with Boulevard, Indianapolis, IN 46202; e-mail: [email protected]; fax: 317-274-5346. respect to the menstrual cycle that (1) can be im- DOI: 10.1097/01.MP.0000039566.20817.46 plemented retrospectively, (2) can capture data re- 1348 garding the ovulatory state of the cycle, and 3) is 2 per case) from these cases. Thirty cases (explor- reliable and reproducible. atory set) were initially analyzed with full knowl- As morphological dating previously has been per- edge of the menstrual dates in order to develop the formed on “normal” autopsy or reduction mammo- morphological criteria. These criteria were then ap- plasty specimens, parameters for assessing men- plied to the entire set of 73 cases in blinded review. strual cycle changes in the breast exist. In this The lobules from the breast tissue of the patients study, we modify these parameters to extend their from the exploratory set were evaluated for the ability to assess menstrual cycle phase in patients following histological features: epithelial and myo- undergoing surgery for benign breast diseases. epithelial distinction; the degree and extent of myo- epithelial cell vacuolation, stromal edema, and stromal infiltrate; sharpness of luminal border; and MATERIALS AND METHODS eosinophilic secretions within the lumina. These Women were recruited at the Breast Center of variables were correlated with menstrual dates to Upstate Medical University (Syracuse, NY) for an generate the final set of criteria to be applied to the ongoing case–control study that aims to correlate entire set. expression of hormone receptors with proliferation Follicular and luteal phase was defined by day of and apoptosis in normal breast. Patients taking oral the cycle after standardizing to a 28-day cycle using contraceptives or hormonal therapy were excluded the last menstrual period and average duration of from this study. The patients included in the cur- cycle information (see above). The menstrual cycle rent analysis are a subset from this study. Detailed was divided into four intervals based on the cyclical obstetrical and menstrual history, including the fluctuations of the estrogen, progesterone, luteal date of the last menstrual period and the usual hormone, and follicular stimulating hormone doc- length of the menstrual cycle, were obtained before umented in previous studies (9–11) rather than their breast surgery. The expected date of the onset weekly intervals determined by calendar dates. of the next menstrual period was computed from Early follicular ranged from Day 0 to Day 5 and late the average length of the cycle and date of the last follicular, from Day 6 to Day 15. Early luteal phase menstrual period. The day of cycle at the time of spanned Day 16 to Day 24, whereas late luteal was breast surgery was then calculated and adjusted to between Day 25 to Day 28. The statistical signifi- a 28-day cycle, assuming that the luteal phase du- cance was examined using the Pearson’s correla- ration is more or less constant (14 d), using the tion test using the Stata program. following formula: adjusted day of cycle RESULTS The age range of the population under study was 14 ϫ day of the cycle at the time of biopsy ϭ 18 to 53 years, with a mean of 36.6 years. The length of the follicular phase commonest of the diagnoses was fibrocystic change (1) followed by fibroadenoma. For example, in a patient who has an average Exploratory Set period length of 32 days, the ovulation is estimated to occur around the 19th day, calculated from the Thirty patients with accurate menstrual cycle in- last menstrual period (follicular phase length ϭ formation in relation to the biopsy date were cho- 18 d, and luteal phase length ϭ 14 d). If the date of sen to establish the morphologic criteria. Histolog- biopsy falls on the 16th day in this cycle, her day in ical features of the lobules evaluated were epithelial the present cycle with respect to a 28-day-cycle and myoepithelial layer distinction; proportion of would be as follows: myoepithelial cells exhibiting vacuolation; degree of myoepithelial vacuolation; sharpness of luminal 14 ϫ 16 border; and presence of eosinophilic luminal secre- ϭ 12.44 days (2) 18 tions, stromal edema, and stromal infiltrate. The presence of apoptotic bodies usually observed to- Inclusion for the purpose of this analysis was ward the basal portion of the luminal cells and restricted to 73 women who did not have breast mitotic figures toward the luminal aspect in lumi- cancer and had at least two normal terminal duct nal cells were also noted. lobular units present in their biopsy material. In 31 Although no single criterion could distinguish of these patients, serum levels of estradiol and pro- follicular from the luteal phase in all cases, there gesterone at the time of surgery were available for were significant differences. Distinct epithelial– correlation. Two pathologists (RR and SB) analyzed myoepithelial layers, stromal edema, and infiltrate hematoxylin and eosin–stained breast sections (1 or were predominantly seen in the luteal phase. Mito- Breast Morphology in Menstrual Cycle (R. Ramakrishnan et al.) 1349 ses were rarely, if ever, noticed in the follicular TABLE 2. Distribution of the Individual Phases by Scores and by Days phase. Both mitoses and apoptotic figures were Scores by Days Phase in frequent in the late luteal phase. However, in a Menstrual Phase Morphology (in Menstrual Cycle) Divisions small percentage of cases, apoptotic bodies were Early follicular 0–50–51 also noted in the early part of the cycle. Using these Late follicular 6–96–15 2 morphological features, it was possible to distin- Early luteal 10–15 16–24 3 guish the 2 phases in all the cases.
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