Yeungnam Univ J Med.  2020 Apr;37(2):90-97. 10.12701/yujm.2019.00353.

Usefulness of subtraction pelvic magnetic resonance imaging for detection of ovarian endometriosis

• Lee HJ

• KMID: 2501415
• DOI: http://doi.org/10.12701/yujm.2019.00353

Abstract

Background
To minimize damage to the ovarian reserve, it is necessary to evaluate the follicular density in the ovarian tissue surrounding endometrioma on preoperative imaging. The purpose of the present study was to evaluate the usefulness of subtraction pelvic magnetic resonance imaging (MRI) to detect ovarian reserve.
Methods
A subtracted T1-weighted image (subT1WI) was obtained by subtracting unenhanced T1WI from contrast-enhanced T1WI (ceT1WI) with similar parameters in 22 patients with ovarian endometrioma. The signal-to-noise ratio (SNR) in ovarian endometrioma, which was classified into the high signal intensity and iso-to-low signal intensity groups on the T2-weighted image, was compared to that in normal ovarian tissue. To evaluate the effect of contrast enhancement, a standardization map was obtained by dividing subT1WI by ceT1WI.
Results
On visual assessment of 22 patients with ovarian endometrioma, 16 patients showed a high signal intensity, and 6 patients showed an iso-to-low signal intensity on T1WI. Although SNR in endometrioma with a high signal intensity was higher than that with an iso-to-low signal intensity, there was no difference in SNR after the subtraction (13.72±77.55 vs. 63.03±43.90, p=0.126). The area of the affected ovary was smaller than that of the normal ovary (121.10±22.48 vs. 380.51±75.87 mm2, p=0.002), but the mean number of pixels in the viable remaining tissue of the affected ovary was similar to that of the normal ovary (0.53±0.09 vs. 0.47±0.09, p=0.682).
Conclusion
The subtraction technique used with pelvic MRI could reveal the extent of endometrial invasion of the normal ovarian tissue and viable remnant ovarian tissue.

Keyword

Endometrioma; Gadolinium; Magnetic resonance imaging; Subtraction

Figure

• 

  Fig. 1. Subtraction imaging and normalization of the contrast-enhanced effect. The ceTIWI (A) is subtracted by the unenhanced T1WI (B) to yield the subT1WI (C). To normalize the effect of contrast enhancement, the subT1WI (C) is divided by the ceT1WI (A) using ImageJ. The normalized perfusion map (D) is scored 0–1. ceT1WI, contrast-enhanced T1-weighted image; subT1WI, subtracted T1-weighted image.

• 

  Fig. 2. Multiple hemorrhagic cysts in a 36-year-old woman with endometriosis. The pre-contrast T1WI with fat suppression (A) and post-contrast T1WI in the arterial phase of enhancement with fat suppression (B) show multiple (arrows) high signal intensities. The subtraction image (C) shows low signal intensity, regardless of the pre-contrast imaging. The number of pixels ranges 0.01–0.12 (arrows) (D). T1WI, T1-weighted image.

• 

  Fig. 3. The T2-weighted image (A) and standardization map of the subtraction image (B) in a woman with endometriosis. The ovary with endometriosis (arrow) displaces the small ovarian follicles (white arrowheads). However, the mean number of pixels in the viable remaining tissue of the ovary with endometriosis is similar to that of the ovary without endometriosis (black arrowheads). Plotting (C) for the uterus, affected ovary, endometriosis, remnant ovary, and normal ovary show similar patterns between the remnant ovary and the normal ovary. The x-axis represents the mean number of pixels (dot) with standard deviation (bar), and the y-axis represents the area (dot) with integral density of the included structure (bar).

Reference

References

1. Hauth EA, Stattaus J, Kimmig R, Schmidt M, Forsting M. Magnetic resonance imaging (MRI) of the pelvis in diagnosing endometriosis. Zentralbl Gynakol. 2005; 127:76–82.

2. Kinkel K, Frei KA, Balleyguier C, Chapron C. Diagnosis of endometriosis with imaging: a review. Eur Radiol. 2006; 16:285–98.

3. Woodward PJ, Sohaey R, Mezzetti TP Jr. Endometriosis: radiologic-pathologic correlation. Radiographics. 2001; 21:193–216.

4. Nishio N, Kido A, Kataoka M, Kuwahara R, Nakao K, Kurata Y, et al. Longitudinal changes in magnetic resonance imaging of malignant and borderline tumors associated with ovarian endometriotic cyst comparing with endometriotic cysts without arising malignancy. Eur J Radiol. 2018; 105:175–81.

5. Tanaka YO, Okada S, Yagi T, Satoh T, Oki A, Tsunoda H, et al. MRI of endometriotic cysts in association with ovarian carcinoma. AJR Am J Roentgenol. 2010; 194:355–61.

6. Sugimura K, Okizuka H, Imaoka I, Kaji Y, Takahashi K, Kitao M, et al. Pelvic endometriosis: detection and diagnosis with chemical shift MR imaging. Radiology. 1993; 188:435–8.

7. Sanchez AM, Viganò P, Somigliana E, Panina-Bordignon P, Vercellini P, Candiani M. The distinguishing cellular and molecular features of the endometriotic ovarian cyst: from pathophysiology to the potential endometrioma-mediated damage to the ovary. Hum Reprod Update. 2014; 20:217–30.

8. Togashi K, Nishimura K, Kimura I, Tsuda Y, Yamashita K, Shibata T, et al. Endometrial cysts: diagnosis with MR imaging. Radiology. 1991; 180:73–8.

9. Bazot M, Bharwani N, Huchon C, Kinkel K, Cunha TM, Guerra A, et al. European society of urogenital radiology (ESUR) guidelines: MR imaging of pelvic endometriosis. Eur Radiol. 2017; 27:2765–75.

10. Forstner R, Meissnitzer M, Schlattau A, Spencer JA. MRI in ovarian cancer. Imaging Med. 2012; 4:59–75.

11. Working group of ESGE, ESHRE, and WES, Saridogan E, Becker CM, Feki A, Grimbizis GF, Hummelshoj L, et al. Recommendations for the surgical treatment of endometriosis-part 1: ovarian endometrioma. Gynecol Surg. 2017; 14:27.

12. Grammatikakis I, Evangelinakis N, Salamalekis G, Tziortzioti V, Samaras C, Chrelias C, et al. Prevalence of severe pelvic inflammatory disease and endometriotic ovarian cysts: a 7-year retrospective study. Clin Exp Obstet Gynecol. 2009; 36:235–6.

13. Guan X, Yu X, Liu X, Long J, Dai J. CT perfusion imaging and CT subtraction angiography in the diagnosis of ischemic cerebrovascular disease within 24 hours. Chin Med J (Engl). 2003; 116:368–72.

14. Lee VS, Flyer MA, Weinreb JC, Krinsky GA, Rofsky NM. Image subtraction in gadolinium-enhanced MR imaging. AJR Am J Roentgenol. 1996; 167:1427–32.

15. Eid M, Abougabal A. Subtraction images: a really helpful tool in non-vascular MRI. Egypt J Radiol Nucl Med. 2014; 45:909–19.

16. American Society for Reproductive Medicine. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril. 1997; 67:817–21.

17. Newatia A, Khatri G, Friedman B, Hines J. Subtraction imaging: applications for nonvascular abdominal MRI. AJR Am J Roentgenol. 2007; 188:1018–25.

18. Hecht EM, Israel GM, Krinsky GA, Hahn WY, Kim DC, Belitskaya-Levy I, et al. Renal masses: quantitative analysis of enhancement with signal intensity measurements versus qualitative analysis of enhancement with image subtraction for diagnosing malignancy at MR imaging. Radiology. 2004; 232:373–8.

19. Yu JS, Rofsky NM. Dynamic subtraction MR imaging of the liver: advantages and pitfalls. AJR Am J Roentgenol. 2003; 180:1351–7.

20. Chanana C, Gupta N, Bansal I, Hooda K, Sharma P, Gupta M, et al. Different sonographic faces of ectopic pregnancy. J Clin Imaging Sci. 2017; 7:6.

21. Bennett GL, Slywotzky CM, Cantera M, Hecht EM. Unusual manifestations and complications of endometriosis--spectrum of imaging findings: self-assessment module. AJR Am J Roentgenol. 2010; 194(6 Suppl):S84–8.

22. Gandhi D, Garg G, Solanki S, Nepal P. Deep infiltrating endometriosis: role of magnetic resonance subtraction imaging. Quant Imaging Med Surg. 2018; 8:722–3.

23. Sun X, Shi L, Luo Y, Yang W, Li H, Liang P, et al. Histogram-based normalization technique on human brain magnetic resonance images from different acquisitions. Biomed Eng Online. 2015; 14:73.

24. Hornstein MD, Gleason RE, Orav J, Haas ST, Friedman AJ, Rein MS, et al. The reproducibility of the revised American Fertility Society classification of endometriosis. Fertil Steril. 1993; 59:1015–21.

25. Schultes G. Classification of endometriosis. Wien Med Wochenschr. 1999; 149:361–5.

26. Chan JH, Peh WC, Tsui EY, Wong KP, Yuen MK. Three-dimensional time-of-flight subtraction angiography of subacute cerebral hemorrhage. AJR Am J Roentgenol. 2003; 181:242–4.

27. Cheng B, Cai W, Sun C, Kang Y, Gong J. 3D bone subtraction CT angiography for the evaluation of intracranial aneurysms: a comparison study with 2D bone subtraction CT angiography and conventional non-subtracted CT angiography. Acta Radiol. 2015; 56:1127–34.

28. Jamil K, Walker T, Onikul E, Munns CF, Little DG. A comparison of subtraction MRI with the standard contrast-enhanced imaging in Perthes' disease. J Child Orthop. 2019; 13:82–8.