Takeshi Kamitani1, Hidetake Yabuuchi2, Mitsuhiro Tozaki3, Yoshihide Kanemaki4, Satoshi Kawanami5, Koji Sagiyama1, Yuzo Yamasaki1, Seitaro Shin1, and Hiroshi Honda1
1Department of Clinical Radiology, Kyushu University, Fukuoka, Japan, 2Department of Health Sciences, Kyushu University, Fukuoka, Japan, 3Department of Radiology, Sagara Hospital Affiliated Breast Center, Kagoshima, Japan, 4Breast and Imaging Center, St. Marianna University School of Medicine, Kawasaki, Japan, 5Department of Molecular Imaging & Diagnosis, Kyushu Universtiy, Fukuoka, Japan
Synopsis
Background
parenchymal enhancement (BPE) on breast contrast MRI is known to be associated
with the menstrual cycle. We conducted a multicenter
study to evaluate the effect of the menstrual cycle on BPE and cancer detectability
by contrast-enhanced breast MRI in an Asian population. The Degrees of BPE
and cancer detectability were assessed quantitatively and qualitatively. BPE were strongest in the proliferative
phase. The detectability of breast cancer was better at the menstrual and
proliferative phases than at secretary phase. Not only the proliferative phase
but also the menstrual phase is suitable for breast MRI examinations of
premenopausal Asian women.
Purpose
Background
parenchymal enhancement (BPE) on breast contrast magnetic resonance imaging (MRI)
is known to be associated with the menstrual cycle 1-3. Prominent BPE could
disturb lesion detection 4,5. Enhancement of normal breast tissue
could result in false-positive findings or even mask a small abnormal enhancing
cancer, resulting in a false-negative report 1. It is thus important
to perform breast MRI at the optimal phases of the menstrual cycle. The
European Society of Breast Imaging guidelines state that the optimal time to perform a breast MRI in premenopausal
women is between the 5th and 12th day after the menstrual cycle’s start 2,
but this is based on studies conducted mostly in Western populations 6-8.
To our knowledge, there are only two single-center studies providing
corresponding Asian data 9,10.
Here we conducted a multicenter study to evaluate
the effect of the menstrual cycle on BPE and cancer detectability by
contrast-enhanced breast MRI in an Asian population.Methods
We enrolled 962 women who underwent breast MRI in
November 2013–March 2015 from 23 centers. The menstrual status was obtained by
interview; 266 premenopausal patients (ages 23–54 yrs, mean 42.4 yrs) with
regular menstrual cycles were included, and 176 of them were diagnosed by
pathology as having breast cancer. Thirty-five patients were examined in the
menstrual phase (days 1–4), 105 in the proliferative phase (days 5–14), and 126
in the secretory phase (days 15–30). For a quantitative assessment, the signal
intensities (SIs) of breast tissue on the unaffected side on a pre-contrast
image (SI1) and an early-phase image (SI2), the SIs of
breast tissue on the affected side on a pre-contrast image (SI3) and
an early-phase image (SI4), and the SIs of breast cancer on a
pre-contrast image (SI5) and an early-phase image (SI6)
were measured. We then calculated, for each patient, the BPE ratio, i.e., (SI2 – SI1)/SI1
and the cancer / background enhancement ratio (C/B ratio), i.e., (SI6 – SI5) / (SI4 – SI3).
We compared the results of the quantitative assessment with the menstrual cycle
using a Kruskal-Wallis analysis. For the qualitative assessment, the BPE was
classified as “minimal ” “mild ” “moderate ” or “marked,” and the cancer detectability
was classified as “excellent ” “good ” or “poor ” independently by two
radiologists. We compared the proportion of minimal-or-mild BPE and that of
excellent-or-good cancer detectability with the menstrual cycle using the chi-squared
test.Results
The
averages of the BPE ratio were 0.25, 0.24, and 0.31 at the menstrual,
proliferative, and secretory phases, with no significant differences among
these values (p=0.21). The averages of the C/B ratio were 20.1, 15.7, and 9.1
at the menstrual, proliferative, and secretory phases (P<0.001). BPE was determined
as moderate or marked in 0% and 5.4% at the menstrual phase, 10.3% and 11.0% at
the proliferative phase, and 17.5% and 21.7% at the secretory phase by the two
observers, respectively (p=0.01, p=0.01). The detectability of breast cancer
was classified as poor in 0% and 0%, 1.4% and 13.0%, and 8.0% and 22.1% at the
menstrual, proliferative, and secretory phases by the two observers,
respectively (p=0.07, p=0.02). Discussion
Breast tissue is influenced by
cyclic hormonal changes, especially estrogen, according to the menstrual cycle 5,10,11.
BPE is therefore influenced by the menstrual cycle. A previous study reported a significant correlation between BPE and
mammographic density 9. Another study reported that the influence of the menstrual cycle on the BPE is
different according to the breast composition, and that the optimal time for
breast MRI could be different for dense and fatty breasts; those authors described that fatty
breasts showed the highest BPE in the 4th week and lowest BPE in the 2nd week of
the menstrual cycle, whereas dense breasts showed the highest BPE in the 3rd
week and the lowest BPE in the 4th week 5. Breast composition varies among racial groups. In
general, the breasts of Asian women are relatively small in size and are commonly
characterized as dense or heterogeneously dense compared to breasts of Western
women 12. Our
present findings demonstrated that not
only the proliferative phase but also the menstrual phase is suitable for determining
the optimal timing for breast MRI examinations. The difference in breast composition between Asian women and Western women might be one of the reasons underlying the present
acceptable result even in the menstrual phase (1st
week).Conclusion
The
menstrual cycle affects BPE and the detectability of breast cancer. Not only the
proliferative phase but also the menstrual phase is suitable for breast MRI
examinations of premenopausal Asian women.Acknowledgements
This study was supported by a grant from Bayer Healthcare.References
1. Ellis RL. Optimal timing of breast MRI examinations
for premenopausal women who do not have a normal menstrual cycle. Am J
Roentgenol AJR2009;193(6):1738-1740.
2. Mann RM, Kuhl CK, Kinkel K, et al. Breast MRI:
guidelines from the European Society of Breast Imaging. Eur Radiol 2008;18(7):1307-1318.
3. Scaranelo AM, Carrillo MC, Fleming R, et al. Pilot
study of quantitative analysis of background enhancement on breast MR images:
association with menstrual cycle and mammographic breast density. Radiology
2013;267(3):692-700.
4. Shin S, Ko ES,
Kim RB, et al. Effect of menstrual cycle and menopausal status on apparent
diffusion coefficient values and detectability of invasive ductal carcinoma on
diffusion-weighted MRI. Breast Cancer Res Treat 2015; 149(3):751-759.
5. Kang SS, Ko EY,
Han BK, et al. Background parenchymal enhancement on breast MRI: influence of
menstrual cycle and breast composition. JMRI 2014;39(3):526-534.
6.
Delille JP, Slanetz PJ, Yeh ED, et al. Physiologic changes in breast magnetic
resonance imaging during the menstrual cycle: perfusion imaging, signal
enhancement, and influence of the T1 relaxation time of breast tissue. Breast J
2005;11(4):236–241.
7.
Kuhl CK, Bieling HB, Gieseke J, et al. Healthy premenopausal breast parenchyma
in dynamic contrast-enhanced MR imaging of the breast: normal contrast medium
enhancement and cyclical-phase dependency. Radiology 1997;203(1):137–144.
8.
Muller-Schimpfle M, Ohmenhauser K, Stoll P, et al. Menstrual cycle and age:
influence on parenchymal contrast medium enhancement in MR imaging of the
breast. Radiology 1997;203(1):145–149.
9. Uematsu T, Kasami M, Watanabe J. Should breast MRI be performed with adjustment for
the phase in patients’ menstrual cycle?
Correlation between mammographic density, age, and background
enhancement on breast MRI without adjusting for the phase in patients’
menstrual cycle. Eur J Radiol 2012;81(7):1539-1542.
10.
Kajihara M, Goto M, Hirayama Y, et al. Effect of the menstrual cycle on
background parenchymal enhancement in breast MR imaging. Magn Reson Med Sci 2013;12(1):39-45.
11. Amarosa AR, McKellop J, Leite APK,
et al. Evaluation of the kinetic properties
of background parenchymal enhancement throughout the phases of the menstrual cycle.
Radiology 2013;268(2):356-365.
12. Takamoto Y, Tsunoda H, Kikuchi M, et
al. Role of breast tomosynthesis in diagnosis of breast cancer for Japanese
women. Asian Pacific J Cancer Prev 2013;14(5):3037-3040.