|Year : 2020 | Volume
| Issue : 10 | Page : 1339-1344
Role of acoustic radiation force-based elasticity imaging in endometrium pathologies
HC Cenkeri1, TB Bidaci2, B Yilmaz1, G Desteli2
1 Department of Radiology, Okan University, Istanbul, Turkey
2 Department of Obstetrics and Gynecology, Baskent University, Istanbul, Turkey
|Date of Submission||19-Nov-2018|
|Date of Acceptance||10-Feb-2020|
|Date of Web Publication||12-Oct-2020|
Dr. H C Cenkeri
Department of Radiology, Okan University Hospital, Içmeler Mahallesi Aydinli Yolu Caddesi No:2 34947 Içmeler/ Tuzla/Istanbul
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Backround: Ultrasonography is difficult to distinguish between endometrial pathologies and often requires curettage. ARFI (Acoustic Radiation Force-Based Elasticity Imaging) is a new ultrasonography elastography method. Using ARFI, it is possible to obtain information about the likelihood of the tissue benign or malignant. Aim: The aim of this study is to evaluate the contribution of ARFI to differentiate endometrial pathologies in hysterectomy specimens. Subjects and Methods: Our study was prospectively, January–May 2017, performed in randomly 45 cases of 41–91 years of age (mean 58.3 years) who have decided to have hysterectomy. Hysterectomy was performed for uterine prolapse and endometrial hyperplasia in elderly patients and menorrhagia in young patients. Pathology results were compared with ARFI values and endometrial thickness. ANNOVA test was used for the comparison of ARFI values. Results: Pathology revealed 14 cases of endometrial atrophy, 11 cases of proliferative phase, 10 cases of polyp, 6 cases of endometrial hyperplasia, and 4 cases of endometrium cancer. There is a statistically significant difference between mean ARFI values of endometrium, subendometrium, and myometrium of the groups (P < 0.05). There was a statistically significant difference between the mean endometrial thickness of the groups (P < 0.05). Conclusion: Endometrium ARFI contributes to the differential diagnosis of endometrial pathologies. Subendometrial and myometrial ARFI values decrease in polyps and increase in hyperplasia. Our study shows that the addition of subendometrium ARFI to gray-scale sonography before deciding on invasive procedures in endometrial pathologies may improve diagnostic accuracy. We concluded that further in vivo studies will establish the usefulness of this technique for preoperative diagnostic measures.
Keywords: ARFİ, endometrium, elastography, ultrasonography
|How to cite this article:|
Cenkeri H C, Bidaci T B, Yilmaz B, Desteli G. Role of acoustic radiation force-based elasticity imaging in endometrium pathologies. Niger J Clin Pract 2020;23:1339-44
|How to cite this URL:|
Cenkeri H C, Bidaci T B, Yilmaz B, Desteli G. Role of acoustic radiation force-based elasticity imaging in endometrium pathologies. Niger J Clin Pract [serial online] 2020 [cited 2020 Nov 28];23:1339-44. Available from: https://www.njcponline.com/text.asp?2020/23/10/1339/297928
| Introduction|| |
ARFI (Acoustic Radiation Force-Based Elasticity in Endometrium) is a new ultrasonography (US) elastography technique that uses short-duration amplified sound waves. Unlike other elastography methods which require manual compression, it is not user-dependent.,, Since different tissues have different elasticity coefficients, the tissues can be evaluated qualitatively and quantitatively. With acquired values, it becomes possible to obtain information about the likelihood of the tissue benign or malignant., ARFI is a cheap, painless, noninvasive method that is easily accepted by patients.,
Postmenopausal bleeding is often the cause of benign pathologies. Hovever, endometrium cancer should be excluded.
90% of endometrium cancer cases seek for medical care due to PMC (postmenopausal bleeding). Initially, an invasive procedure, curettage, was used to evaluate PMC cases. Transvaginal ultrasonography (TVUS) has widespread use for initial evaluation because it is noninvasive, inexpensive, safe and can be carried out in a short time and is repeatable. However, it may cause infection and bleeding, and the patient may not accept the examination.
The objective of our study is to demonstrate the contribution of ARFI in distinguishing endometrium pathologies. Its use in endometrium is not found, except for a few studies in the literature.
| Subjects and Methods|| |
Our study was prospectively, January–May 2017, performed in 45 cases of 41–91 years of age (mean 58.3 years) who were admitted to the obstetrician's gynecology clinic with complaints such as uterine prolapse, menorrhagia, metrorrhagia, postmenopausal haemorrhage, and who were decided to have a hysterectomy. This study was approved by the Baskent University ethics committee. G-power analysis (G*Power 3.0.10) was used to determine the sample power. Accordingly, the number of samples detected for power 0.80 and a: 0.05 was calculated as a minimum of 35.
Hysterectomy materials were examined with ARFI, during the operation, before being delivered to pathology and before formalin was applied. ARFI examination was performed with a Siemens S300 device (Siemens, Erlangen, Germany) with V9-4 MHz probe. In the color scale elastography images obtained by eSie Touch EI method, the softness of the tissues was indicated with red and blue color images were obtained as the hardness of the tissues increased; the soft tissues were coded with red and hard tissues were coded with blue. The ROI (region of interest) was placed in the endometrium, submucosal, and myometrial area in the images obtained with the color scale. The ROI used for the measurement is standard size.
Endometrium thickness was measured during the examination. At least 10 measurements were performed along the endometrium corpus and fundus of uterus and minimum, maximum, and mean values were determined. Myometrium homogeneity was evaluated and patients with submucosal myoma were excluded. At least five measurements were made from the submucosal and myometrium, and mean values were calculated. The mean ARFI values and endometrium thickness were compared with pathology results.
All measurements were performed by two radiologists with a long experience of 10 years in the US, blind to the pathology results.
| Statistics|| |
SPSS (Statistical Package for Social Sciences) version 15.0 for Windows (SPSS Inc., Chicago, USA) was used for statistical evaluations. It was assessed whether the data exhibited a normal distribution according to Kolmogorov–Smirnov and Shapiro–Wilk and whether they could be subjected to nonparametric tests. ANNOVA test was used for comparison of atrophic endometrium, proliferative endometrium, endometrial hyperplasia and endometrial cancer mean ARFI values and endometrium thickness. T-test was used to compare the mean ARFI values of the two radiologist.
| Results|| |
Pathology revealed 14 cases of endometrial atrophy, 11 cases of secretory and proliferative phase, 10 cases of polyp, 6 cases of endometrial hyperplasia, and 4 cases of endometrium cancer. Four of the cases have breast cancer stories.
Two of the seven cases (15.5%) with endometrial hyperplasia (EH) had complex atypia (4.4%), one had endometrial intraepithelial neoplasia (2.2%), one had atypical simple EH (2.2%), one had focal atypical simple hyperplasia (2.2%), and one had simple EH (2.2%) without atypia.
Endometrium carcinoma (8.8%) was detected in four out of 45 cases with squamous differentiation in two, one endometriod type and one serous type. Only one of them was in the premenopausal period and the others were in the postmenopausal period. Myometrial invasion was present in all cases and was >50%.
The statistical average of endometrium ARFI values (SD) for the 4 endometrium cancer was 3.34 (1.45) m/s [Figure 1]. In the 10 cases with polyps detected in endometrium, the mean endometrium ARFI value was 3.15 (0.68) m/s [Figure 2]. In the 14 cases with endometrium cases with atrophy, the mean endometrium ARFI value was 3.06 (0.55) m/s. In 11 cases with proliferation detected in endometrium, the endometrium ARFI values averaged 3.62 (1.22) m/s [Figure 3]. In 6 cases with endometrial hyperplasia, endometrium ARFI values averaged 4.05 (0.48) m/s [Figure 4].
There was a statistically significant difference in the mean endometrium ARFI values of the groups (P < 0.05). The endometrial hyperplasia mean endometrium ARFİ values were highest. The average endometrium ARFİ values in atrophic endometrium were lowest. The endometrium ARFI values in endometrial polyps were higher than atrophic endometrium. The endometrial cancers' ARFI values were lower than proliferative endometrium. In our study, no significant difference between cancer and other groups was detected [Table 1].
The statistical average of subendometrial ARFI values (SD) for the 4 endometrium cancer was 3.13 (1.41) m/s. In the 10 cases with polyps detected in endometrium, the mean subendometrial ARFI value was 2.95 (0.46) m/s. In the 14 cases with endometrium cases with atrophy, the mean subendometrial ARFI value was 3.13 (0.91) m/s. In 11 cases with proliferation detected in endometrium, the subendometrial ARFI values averaged 3.80 (1.19) m/s. In 6 cases with endometrial hyperplasia, subendometrial ARFI values averaged 4.14 (0.37) m/s.
There was a statistically significant difference in the mean subendometrial ARFI values of the groups (P < 0.05). ARFI values of subendometrial in the endometrial hyperplasia and proliferation were higher than the other groups. ARFI values of subendometrium were lowest in endometrial polyps. Subendometrial ARFI values are close to endometrial cancer and atrophy cases.
The statistical average of myometrium ARFI values (SD) for the 4 endometrium cancer was 3.53 (0.68) m/s. In the 10 cases with polyps detected in endometrium, the mean myometrium ARFI value was 2.86 (0.58) m/s. In the 14 cases with endometrium cases with atrophy, the mean myometrium ARFI value was 3.52 (0.72) m/s. In 11 cases with proliferation detected in endometrium, the myometrium ARFI values averaged 3.92 (1.19) m/s. In 6 cases with endometrial hyperplasia, myometrium ARFI values averaged 3.60 (0.75) m/s.
There was a statistically significant difference in the mean myometrium ARFI values of the groups (P < 0.05). The mean myometrium ARFİ values of proliferative endometrium were highest. Myometrium ARFI values are close to endometrial cancer and atrophy cases. In endometrial polyps, mean myometrium ARFI values were lower than other groups.
The average endometrium thickness (SD) was found to be 2.00 (1.35) mm for atrophy, 2.90 (1.28) mm for endometrial proliferation, 2.66 (2.17) mm for polyp, 2.16 (0.75) mm for hyperplasia, and 6.00 (4.00) mm for cancer. There is a statistically significant difference between the mean endometrium thickness of cancer and the other groups (P < 0.01). The mean endometrial thickness, in TVUS, before hysterectomy was found to be 5.92 (3–20) mm for atrophy, 5.87 (4–7) mm for endometrial proliferation, 7.66 (3–16) mm for polyp, 4 (3–5) mm for hyperplasia, and 15.25 (14-16) mm for cancer.
There was statistically difference between the mean ARFI values of the two radiologists (P < 0.01).
| Discussion|| |
Elastography is an examination that can be performed as part of a combination of physical examination and sonographic imaging where the main purpose is to identify tissue strain. One of the most common methods in use is observing the tissue strain by the variety of colors, where red denotes the greatest strain (softest) and blue denotes the tissue with no strain (hardest). This method has been in wide use for breast, thyroid, and liver diseases in recent years (1-11).
ARFI is a US elastography method. Unlike other US elastography methods, it is not user-dependent because it does not need probe pressure., Since malignant lesions are harder and more rigid than benign lesions, they tend to translocate less. Our study can also be seen as a new case study for ARFI in endometrial pathologies in vitro. We chose to apply ARFI technology in addition to conventional elastography to observe more non-user dependent values, and we chose an in vitro study to eliminate the possible effect of subcutaneous fatty tissue on the penetration of sound waves with a transabdominal probe.
Atypia is the most important prognostic factor in EH cases. The risk of progression to cancer in atypical EH, approximately 14 times more. The incidence of concurrent endometrial cancer in atypical endometrial hyperplasia is reported to be 34.3%. For these reasons, cases with atypical endometrial hyperplasia were included in the cancer group.
In our study, we evaluated the contribution of endometrium cancer, no significant difference between cancer and other groups were detected. However, endometrial hyperplasia mean endometrium ARFİ values were highest.
Similarly, the endometrial tissue strain ratio was found to be significantly increased in cases with endometrial pathologies in women using Tamoxifen for breast cancer.
In the study Metin et al. conducted by TVUS strain elastography, elasticity increased in cases with endometrium cancer when compared to control and hyperplasia group.
İn Gültekin et al. study, where they compared endometrium thickness and strain ratios in elastography (TVUS), in cases of endometrial hyperplasia or polyp, the strain rates were significantly reduced compared to the normal group. This method is largely dependent on examiner's experience in strain elastosonography.
In TVUS ARFI, when an amplified wave with a frequency lower than 7 MHz is used, sufficient translocation in the cervix can be achieved. Sound waves with higher frequencies cause shift artefacts toward the probe in which they are generated. However, while the use of higher frequency sound waves leads to more translocations in hard tissues, the amplified sound wave can be extended to the depth of about 2 mm in the axial plane forward. This is the limitation of TVUS ARFI.
Shear wave elastography is a promising adjunct to TVUS for evaluation of the uterus, and the results from this study may provide normal data, which may further help diagnosing various uterine diseases.
In our study, the endometrium thickness in the endometrium cancer group was statistically significantly increased. 70% of the cases occur in postmenopausal period with thickening in the endometrium., The endometrium cancer may be diffused, focal, or nodular.,, For this reason, only endometrial thickness measurement may not be sufficient to diagnose endometrium cancer.
In our study, the mean myometrium ARFİ values of proliferative endometrium were highest. ARFI values of subendometrium and myometrium were lowest in endometrial polyps. ARFI values of subendometrial in the endometrial hyperplasia and proliferation were higher than the other groups. We think that subendometrial and myometrium ARFI values decrease in polyps and increase in hyperplasia and contribute to differential diagnosis.
Wozniak evaluated two cases of submucosal fibroid and endometrial polyp by TVUS strain elastography. Similarly, the endometrial polyp was reported to be softer than the myometrium and endometrium.
In the literature, there are no studies involving this number of cases of endometrial pathologies previously performed with ARFI. This is the advantage of our study. Distance is important in elastography examinations. The distance between the probe and the endometirum increases in TVUS and transabdominal US examinations. If strain or shear wave technology is used, its effectiveness is reduced. Therefore, our study was performed in vitro. Since the endocavitary probe did not have ARFI option, preoperative TVUS ARFI evaluation was not possible. This is the limitation of our study. One of the weaknesses of our study is the low number of endometrial cancer cases. The advantage of our study is that ARFI, which is the method we used compared to previous studies with strain elastography in the literature, is not quantitative and user-dependent. In addition, the ability to sample along the entire endometrium line is an advantage of our study.
In conclusion, ın vitro measurements of endometrium and subendometrium ARFI of the endometrial pathologies were found to show a significant difference. However, it is insufficient to distinguish cancer from other pathologies. Our study shows that the addition of subendometrium ARFI to gray-scale sonography before deciding on invasive procedures in endometrial pathologies may improve diagnostic accuracy. We concluded that further in vivo studies will establish the usefulness of this technique for preoperative diagnostic measures.
Financial support and sponsorship
Conflicts of Interest
There are no conflicts of interest.
| References|| |
Kathy Nightingale. Acoustic radiation force impulse (ARFI) imaging: A review. Curr Med Imaging Rev 2011;7:328-39.
Sporea I, Sirli R, Bota S, Popescu A, Sendroiu M, Jurchis A. Comparative study concerning the value of acoustic radiation force impulse elastography (ARFİ) in comparison with transient elastography (TE) for the assessment of liver fibrosis in patients with chronic hepatitis B and C. Ultrasound Med Biol 2012;38:1310-6.
Sporea I, Sirli R, Bota S, Popescu A, Badea R, Lupsor M, Focsa M, et al
. İs it better to use together transient elastography (TE) and acoustic radiation force impulse elastography (ARFİ) for fibrosis evaluation in patients with chronic HCV hepatitis? Gastroenterology 2010;140(Suppl):S968.
Lees WR. Acoustic radiation force imaging: A new method for quantifying hepatic fibrosis. Eur Radiol2009;19:s308.
Boursier J, Isselin G, Fouchard-Hubert I, Oberti F, Dib N, Lebigot J, et al
. Acoustic radiation force impulse: A new ultrasonografic technology for the wide-spread noninvasive diagnosis of liver fibrosis. Eur J Gastroenterol Hepatol 2010;22:1074-84.
Galloti A, D'Onofrio M, Romanini L, Cantisani V, Pozzi Mucelli R. Acoustic radiation force impulse (ARFİ) ultrasound imaging of solid focal liver lesions. Eur J Radiology 2012;81:451-5.
Allen JD, Ham KL, Dumont DM, Sleshi B, Trahey GE, Dajl J. The development and potential of acoustic radiation force impulse (ARFİ) imaging for carotid artery plaque characterization. J Vasc Med 2011;16:302-11.
Bakour SH, Timmermans A, Willem Mol B, Khan KS. Management of women with postmenopausal bleeding: Evidence-based review. Obstet Gynaecol 2012;14:243-9.
Su Y, Du L, Wu, Zhang J, Zhang X, Jia X, et al
. Evaluation of cervical cancer detection with acoustic radiation force impulse ultrasound imaging. Experimental and Therapeutic Medicine 2013;5:1715-9.
Özkaya E, Korkmaz V, Özkaya Y, Tosun A, Küçükozkan T, Bostan H. Ultrasonographic endometrial thickness measurement is predictive for treatment response in simple endometrial hyperplasia without atypia. J Turkish-German Gynecol Assoc 2013;14:19-22.
Tanter M, Bercoff J, Athansiou A, Deffieux T, Gennison J, Montaldo G, et al
. Quantitative assessment of breast lesion viscoelasticity: Initial clinical results using supersonic shear imaging. Ultrasound Med Biol 2008;34:1373-86.
Metin MR, Aydın H, Ünal Ö, Akçay Y, Duymuş M, Türkyılmaz E, et al.
Differentiation between endometrial carcinoma and atypical endometrial hyperplasia with transvaginal sonographic elastography. Diagn Interv Imaging 2016;97:425-31.
Kurman RJ, Kaminski PF, Norris HJ. The behavior of endometrial hyperplasia. A long-term study of “untreated” hyperplasia in 170 patients. Cancer 1985;56:403-12.
Salman MC, Usubutun A, Dogan NU, Yuce K. The accuracy of frozen section analysis at hysterectomy in patients with atypical endometrial hyperplasia. Clin Exp Obstet Gynecol 2009;36:31-4.
Gultekin IB, Imamoglu GI, Gultekin S, Yilmaz EA, Yilmaz Z, Alkan A, et al.
Elastosonographic evaluation of endometrium in women using tamoxifen for breast cancer. Niger J Clin Pract 2019;22:92-100.
] [Full text]
Gultekin IB, Imamoglu GI, Turgal M, Gultekin S, Öcal FD, Alkan A, et al
. Elastosonographic evaluation of patients with a sonographic finding of thickened endometrium. Eur J Obstet Gynecol Reprod Biol 2016;198:105-9.
Palmeri ML, Feltovich H, Homyk AD, Carlson LC, Hall TJ. Evaluating the feasibility of acoustic radiation force impulse shear wave elasticity imaging of the uterine cervix with an intracavity array: A simulation study. IEEE Trans Ultrason Ferroelectr Freq Control 2013;60:2053-64.
Manchanda S, Vora Z, Sharma R, Hari S, Das CJ, Kumar S, et al
. Quantitative sonoelastographic assessment of the normal uterus using shear wave elastography: An initial experience. J Ultrasound Med 2019;38:3183-9.
Goldstein SR. Use of ultrasonohysterography for for triage of perimenopausal patients with unexplained uterine bleeding. Am J Obstet Gynecol 1994;170:565-70.
Long CA. Evaluation of patients with abnormal uterine bleeding. Am J Obstet Gynecol 1996;175:784-6.
Yasa C, Dural O, Bastu E, Ugurlucan FG, Nehir A, İyibozkurt AC. Evaluation of the diagnostic role of transvaginal ultrasound measurements of endometrial thickness to detectendometrial malignancy in asymptomatic postmenopausal women. Arch Gynecol Obstet 2016;294:311-6.
Gultekin IB, Imamoglu GI, Turgal M, Gultekin S, Öcal FD, Alkan A, et al
. Elastosonographic evaluation of patients with a sonographic finding of thickened endometrium. Eur J Obstet Gynecol Reprod Biol 2016;198:105-9.
Wozniak S. The potential role of elastography in differentiating between endometrial polyps and submucosal fibroids: A preliminary study. Menopause Review Przeglad Menopauzalny 2015;14:130-3.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]