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CONCLUSION. There was no evidence of a difference in outcomes of screening MRI examinations as a function of the week of menstrual cycle in which the study is performed.
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Read More »The use of MRI as an adjunctive screening tool for women at high risk for breast cancer has been increasing. In a study of trends in breast MRI utilization in the United States, examinations performed for high-risk screening were uncommon in the year 2000 but constituted more than half of all breast MRI examinations in 2011 [1]. This increase is largely because of a combination of the recognition of the limitations of mammography, particularly in high-risk populations, and the high sensitivity of breast MRI for cancer detection [2, 3]. To be maximally effective, however, a screening test should have high specificity along with high sensitivity, with as few false-positives as possible, while detecting a high percentage of cancers present. Breast MRI was recognized early in its use as having high sensitivity for breast cancer, especially for invasive disease [3]. The range of reported specificities of breast MRI, however, varied widely, and this was cited as a disadvantage to breast MRI compared with mammography [4, 5]. Early in the experience with breast MRI, it was recognized that normal breast parenchyma can enhance and that the amount and degree of enhancement can vary with the menstrual cycle in premenopausal women, being lowest in week 2 and in days 7–20 days [6, 7]. In theory, minimizing normal background enhancement should increase the accuracy of MRI interpretation, and the practice of performing screening breast MRI in week 2 of the menstrual cycle, based largely on these early reports, has become widely adopted. The American College of Radiology (ACR) practice parameter for breast MRI states the following [8]: Increased parenchymal enhancement has been observed normally during the secretory phase of the menstrual cycle. This normal enhancement may give rise to false-positive and false-negative MRI scans. It is therefore recommended that breast MRI scans be performed during the second week of the menstrual cycle for patients undergoing screening examinations. Despite the acknowledged occurrence of increased enhancement of breast tissue at times other than week 2 of the menstrual cycle, the association of the week of the menstrual cycle with actual outcome of the screening MRI examinations in clinical practice has not been well evaluated. The purpose of this study was to determine whether there is any difference in outcomes of screening MRI examinations in premenopausal women as a function of the week of the menstrual cycle in which the study was performed. Materials and Methods Choose Top of page ABSTRACT Materials and Methods << Results Discussion References CITING ARTICLES Study Population This HIPAA-compliant retrospective study was approved by the institutional review board, and the requirement for informed consent was waived. The radiology database was queried to find all breast MRI examinations performed of women 21–55 years old in the 24-month period from January 1, 2011, through December 31, 2012. Cases were included if the indication for the MRI was screening for women at increased risk for breast cancer, the patient was still menstruating, and the date of the 1st day of the last menstrual period was clearly stated. Cases were excluded if the indication for the examination was for any reason other than screening. At our facility, the protocol is to ask patients before each MRI examination to give the date of the 1st day of the last menstrual cycle and this date is recorded by the technologist. However, for many cases no date was recorded, likely because the patient was postmenopausal, or the recorded date was imprecise (e.g., last week, 1 or 2 weeks ago). For this study to be as accurate as possible, we included only cases in which the exact date of the 1st day of the last menstrual period was specifically documented in the MRI report. At our facility, there is no specific requirement to schedule screening MRI examinations during any particular week of the menstrual cycle, but some referring clinicians will try to schedule during week 2 of the menstrual cycle if possible. For purposes of analysis, week 1 was considered days 1–7; week 2, days 8–14; week 3, days 15–21; and week 4, days 22 and greater. Breast MRI Technique All images were acquired with a 1.5- or 3-T MRI system (Signa or Signa HDX, GE Healthcare). In all patients, a dedicated 8-channel (Vantage, GE Healthcare) or 16-channel (Sentinelle, Hologic) surface breast coil was used. Sequences included a localizing sequence, a sagittal fat-suppressed T2-weighted sequence (TR/TE, 4000/85; slice thickness, 3 mm; gap, 1 mm), and a sagittal T1-weighted 3D fast spoiled gradient-echo sequence (flip angle, 35°; bandwidth, 32 kHz; FOV, 18–22 cm; matrix, 192 × 256; slice thickness, 3 mm; gap, 0 mm) before and three times after a rapid bolus injection of 0.1 mmol/kg of gadopentetate dimeglumine (Magnevist, Bayer Health-Care Pharmaceuticals). Subtraction of the first contrast-enhanced sequence was performed, and subtracted maximum-intensity-projection (MIP) images were routinely generated. MRI Interpretation and Review of Reports All studies were interpreted by one of 19 dedicated breast imagers with between 2 and 16 years of experience in reading breast MRI examinations. Each radiologist interpreted between six and 185 of the examinations included in this study, with nine radiologists interpreting fewer than 50 examinations each and the remaining 10 radiologists interpreting 81% of the cases. At our facility, radiology reports are generated by a voice recognition system using standard templates. For each case, the indication for the examination, the dates of any comparison studies, and the technical factors in image acquisition are reported. It has been customary practice at our institution to include a descriptor of the degree of background parenchymal enhancement (BPE) in every MRI report, even before the 5th edition of ACR BI-RADS Atlas [9], which includes these descriptors, was published. BPE was determined by the interpreting radiologist at the time of original reading and was rated as minimal, mild, moderate, or marked. BPE was generally assessed on either the subtraction images from the first contrast-enhanced sequence or the subtracted MIP image. If BPE was different for the two breasts, the highest degree of BPE was assigned. For purposes of analysis, cases with minimal and mild BPE were combined and compared with cases with moderate and marked BPE combined. In the MRI report, any findings were then described, and an impression, management recommendation, and BI-RADS final assessment were given. Variables recorded for each examination included patient age, indication for the examination, date of the last menstrual period, breast composition, degree of BPE, findings, and final BI-RADS assessment. The results of subsequent biopsy and subsequent breast imaging, if performed, were recorded. If a mammographic or sonographic correlate to a suspicious MRI finding was found, biopsy was performed with stereotactic or ultrasound guidance, respectively. MRI-guided biopsies were performed on a 1.5-T magnet (Signa) using a 9-gauge vacuum-assisted device (ATEC, Hologic). The results of follow-up imaging and any biopsy were determined to calculate outcome measures, including sensitivity, specificity, positive predictive values (PPVs), and cancer detection rate (CDR). These measures were determined for all cases and were compared as a function of the week of the menstrual cycle. In addition, the outcomes of cases in week 2 was compared with the outcomes of cases in weeks 1, 3, and 4 combined. It has been reported that tamoxifen decreases BPE [10], and in an attempt to eliminate a possible confounding factor, these outcomes were also analyzed after excluding women who were on tamoxifen. In addition, outcomes of cases with a prior screening MRI examination were compared with those of cases without prior examinations. Statistical Analysis We examined associations between the week of menstrual cycle in which the study was performed and BPE, BI-RADS assessment, and presence of a prior examination. Considering that patients can undergo multiple screening examinations during 2 years, the Rao-Scott chi-square test was used to take into account within-patient correlation. Examinations with BI-RADS 1 or 2 assessments were considered negative, and those with BI-RADS 3, 4, or 5 assessments were considered positive. True-negative examinations were those given a BI-RADS 1 or 2 in which no cancer was found within 365 days or at the next routine screening MRI. True-positive examinations were those given a BI-RADS 3, 4, or 5 in which cancer was diagnosed within the same time frame and at the same location. False-negative examinations were those given a BI-RADS 1 or 2 in which a cancer was diagnosed within 365 days or before the next routine screening MRI and those given a BI-RADS 3, 4, or 5 but a cancer was diagnosed only at a different location within the same time frame. False-positive examinations were those given a BI-RADS 3, 4, or 5 in which no cancer was diagnosed within 365 days. We estimated PPV1 in patients with a positive screening result (BI-RADS 3, 4, or 5), PPV2 and PPV3 in patients assigned a BI-RADS 4 or 5, CDR of the entire cohort, and the specificity in patients with at least 1-year imaging follow-up by the week of the menstrual cycle in which the study was performed and compared estimates using the Rao-Scott chi-square test. Modified 95% CIs were estimated for the outcomes using the Clopper-Pearson approach. The sensitivity in patients with at least 1-year imaging follow-up was estimated and compared using the Fisher exact test considering that all patients included in this analysis were independent. The exact binomial CIs were estimated for sensitivities. These comparisons were also performed between screenings performed during week 2 versus those performed in weeks 1, 3, and 4 combined. All statistical analyses were performed using a software package (SAS, version 9.4, SAS Institute). Results Choose Top of page ABSTRACT Materials and Methods Results << Discussion References CITING ARTICLES During the study period, 5591 breast MRI examinations were performed among premenopausal women 21–55 years old. Of these 5591 MRI examinations, 3715 were performed for high-risk screening; of those 3715 examinations, 1536 examinations of 1239 patients had the date of the 1st day of the last menstrual cycle recorded. These 1536 cases (1239 women) comprise the study population. Among these 1536 cases, two screening MRI examinations were performed in 297 patients, and the remaining patients had a single examination. No patient had more than two studies. All examinations were bilateral with the exception of 176 in which a unilateral study was performed in women who had had a mastectomy. Patient age ranged from 22 to 55 years with a mean of 42.4 years. Of the 1536 MRI studies, 21.8% (n = 335) were performed in menstrual cycle week 1, 35.4% (n = 544) in week 2, 23.4% (n = 360) in week 3, and 19.3% (n = 297) in week 4. All examinations were performed for screening of women with an increased risk for breast cancer. In 696 (45.3%) MRI examinations, the primary risk factor was a 20% or greater lifetime risk by virtue of a family history of breast cancer as determined by the Tyrer-Cusick model. In 551 (35.9%) MRI examinations, the primary risk factor was a personal history of breast cancer. Of these 551 patients, 169 had had mastectomy, and the remaining 382 had been treated with lumpectomy and radiation. Other primary risk factors were a previous biopsy-proven high-risk lesion such as atypical ductal hyperplasia or lobular carcinoma in situ in 152 (9.9%) MRI examinations, a history of chest radiation for treatment of Hodgkin disease in 73 (4.8%), and a known BRCA mutation carrier in 64 (4.2%); 124 women were taking tamoxifen at the time of the MRI examination. Patient age and primary risk factor of the study population as a function of the week of the menstrual cycle in which MRI was performed are listed in Table 1. View Larger Version TABLE 1: Age and Primary Risk Factors by Week of Menstrual Cycle Overall, a prior screening MRI examination had been performed in 1252 of 1536 cases (81.5%). Significantly fewer cases with MRI performed in week 2 had a prior screening MRI examination (77.0%, 419/544 [95% CI, 73.2–80.5%]) compared with those with MRI performed in weeks 1, 3, and 4 (84.0%, 833/992 [95% CI, 81.5–86.2%]) (p = 0.001). BPE was minimal or mild in 737 (48.0%) cases and moderate or marked in 799 (52.0%). This nearly equal distribution of BPE between minimal and mild compared with moderate and marked held true for examinations performed in each week. There was no significant difference in BPE as a function of the week of the menstrual cycle in which MRI was performed with a p value of 0.779 (Table 2). View Larger Version TABLE 2: Background Parenchymal Enhancement (BPE) and BI-RADS Category by Week of Menstrual Cycle There was no significant difference in final BI-RADS assessment category by week of the menstrual cycle (p = 0.137) (Table 2). Most cases were assigned a BI-RADS final assessment category of 1 or 2 (81.8%, 1257/1536). Cases with MRI performed in week 1 had the highest proportion of BI-RADS 1 or 2 readings at 82.9% (278/335), and cases with MRI performed in week 4 had the lowest at 80.5% (239/297). A total of 108 of 1536 (7.0%) cases were assigned BI-RADS 3. Follow-up MRI was available for of these 102 cases, and the first follow-up MRI examination was performed at a mean of 8 months (range, 1–55 months). The mean total length of follow-up of these 102 cases was 39 months (range, 6–63 months). Biopsy was performed in 11 cases because of change detected at follow-up, and malignancy was diagnosed in two of these 11 cases (1.8% of 108 BI-RADS 3 cases). The initial MRI examination of these two cases that subsequently proved to be malignant was performed during week 1 in one patient and during week 2 in the other patient. A BI-RADS 4 or 5 assessment with the recommendation for biopsy occurred in 171 of 1536 (11.1%) cases. Information on subsequent biopsy was available for 154 cases of which 39 were malignant, which yielded a PPV1 of 15% (95% CI, 11–20%), PPV2 of 24% (95% CI, 17–31%), and PPV3 of 25% (95% CI, 18–33%). There was no significant difference in PPV1, PPV2, or PPV3 as a function of the week of the menstrual cycle (Table 3). View Larger Version TABLE 3: Positive Predictive Values (PPVs), Cancer Detection Rate (CDR), Sensitivity, and Specificity Overall and by Week of Menstrual Cycle A total of 41 cancers were detected on MRI among the 1536 examinations, giving a CDR of 27/1000 (95% CI, 19–36/1000). There were 27 invasive cancers and 14 cases of ductal carcinoma in situ (DCIS). The highest CDR occurred in week 3 at 39/1000 (95% CI, 21–64/1000) and lowest in week 4 at 20/1000 (95% CI, 7–43/1000). Rates for weeks 1 and 2 were intermediate at 21/1000 (95% CI, 8–43/000) and 26/1000 (95% CI, 14–43/1000), respectively. However, there was no statistically significant difference in CDR among the menstrual cycle weeks (p = 0.392) (Table 2). When outcomes of cases with MRI performed in week 2 were compared with outcomes of cases with MRI performed in weeks 1, 3, and 4 combined, there was no significant difference in BPE, BI-RADS final assessment category, CDR, PPV1, PPV2, or PPV3 (Table 4). The p value for BI-RADS assessment approached significance at 0.072. More cases with MRI performed in week 2 were assigned BI-RADS 3 and fewer were assigned BI-RADS 4 or 5, but this difference did not meet statistical significance. View Larger Version TABLE 4: Outcomes of Menstrual Cycle Week 2 Compared With Outcomes of Menstrual Cycle Weeks 1, 3, and 4 Combined Follow-up imaging examinations and clinical information of at least 12 months (range, 12–63 months; mean, 40 months) were available for 1415 cases. On follow-up, four false-negative cases, defined as cancers diagnosed within 1 year of a negative finding on screening MRI, were discovered. In all four cases, the indication for MRI was high-risk screening because of a personal history of breast cancer, and all four patients were found to have DCIS seen as calcifications on routine mammography performed from 1 day to 12 months after MRI. One of the false-negative MRI examinations was performed in week 2 and the other three were performed in week 3. Two of the false-negative MRI examinations were given an initial BI-RADS 4 assessment. Both patients underwent MRI-guided biopsy with benign results, and both were found on subsequent routine mammograms to have new calcifications in a completely different quadrant from the MRI finding, which proved to be DCIS. These two cases were counted as false-negative examinations despite the initial BI-RADS 4 assignment because the DCIS in both cases was in a different location from the MRI finding. The overall sensitivity of MRI was 0.91 (41/45; 95% CI, 0.79–0.98) and was not statistically different between weeks of the menstrual cycle. The specificity of MRI for the entire group was 0.84 (95% CI, 0.82–0.86) and was also not statistically different as a function of the week of the menstrual cycle in which MRI was performed. When the sensitivity and specificity of MRI for cases with MRI performed during week 2 were compared with those performed during weeks 1, 3, and 4 combined, there was no significant difference. These results are presented in Table 4. After exclusion of the 124 MRI examinations performed of women on tamoxifen, there was still no significant difference in CDR (p = 0.418), sensitivity (p = 0.494), specificity (p = 0.385), PPV1 (p = 0.213), PPV2 (p = 0.474), or PPV3 (p = 0.511) among women as a function of the week of the menstrual cycle in which MRI was performed. When the outcomes of cases with prior screening MRI examination were compared with those of cases without a prior MRI examination, the CDR was higher among cases without a previous study than among cases with a previous study (44/1000 vs 23/1000; p = 0.053). Specificity was lower for cases without a prior MRI examination compared with those with a prior MRI examination (61% vs 87%; p < 0.001). No significant difference in sensitivity, specificity, or CDR as a function of week of the menstrual cycle was observed in cases with a prior MRI examination and in those without a prior examination.
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