Iranian Society of Gynecology Oncology

Document Type : Review Article

Authors

1 Department of Radiology, Advanced Diagnostic and Interventional Radiology Research Center (ADIR), Medical Imaging Center, Imam Khomeini Complex Hospital, Tehran University of Medical Sciences, Tehran, Iran

2 Department of Radiology, Advanced Diagnostic and Interventional Radiology Research Center (ADIR), Medical Imaging Center, Imam Khomeini Complex Hospital, Tehran, [email protected]

3 Department of Obstetrics and Gynecology Obstetrics & Gynecologist, Faculty of Medicine, Tehran University of Medical Science, Women Hospital (Yas / Mirza Kochak Khan), Tehran, Iran

4 Department of Reproductive Biology Department of Advanced Medical Sciences & Technologies, School of Medicine Jahrom University of Medical Sciences, Jahrom, Iran

5 Department of Radiology, Advanced Diagnostic and Interventional Radiology Research Center (ADIR), Medical Imaging Center, Imam Khomeini Complex Hospital, Tehran university of medical science, Tehran, Iran Department of radiology, Yas women hospital, Tehran university of medical science, Tehran, Iran

Abstract

Diagnosis of endometriosis according to TVS may be an appropriate alternative method for laparoscopy. Hence in this study, the role of TVS was investigated compared with laparoscopic assessment in cases with pelvic endometriosis attending to imaging center of Imam-Khomeini and Yas Hospital in Tehran in 2018. In this diagnostic study, 69 patients with pelvic endometriosis were assessed. The results of TVS were compared with laparoscopic assessment, and the sensitivity, specificity, and congruence rate were determined. According to the obtained results, it may be concluded that most sensitivity of TVS is related to the torus uterinus and dome of the bladder. Also, the most specificity is related to bladder, sigmoid colon, and peritoneal cyst. The most congruence rate between U/S and laparoscopy is at bladder trigon and sigmoid colon. However, in the end, multicenter studies with more cases and comparisons with the results of other diagnostic methods are recommended to achieve more accurate results.

Keywords

Main Subjects

Introduction
 


The presence of endometrial tissue, including the stroma and glands outside the uterus, is called endometriosis. Due to the association of the disease with estrogen in the body, endometriosis is mainly observed in women of childbearing age and sometimes in adolescents and postmenopausal women undergoing hormone replacement therapy (1, 2, 3, 4). About 10% of women of childbearing age suffer from endometriosis, which causes dysmenorrhea, dyspa-reunia, chronic pelvic pain, and infertility (5, 6, 7). Endometriosis is a benign disease of women that often presents with pelvic pain and infertility (7, 8).
About 17 to 44% of patients with endometriosis have ovarian endometrioma (5, 7, 8). Ovarian endometrioma is one of the most common causes of pelvic pain and one of the most common ovarian cysts that we encounter during surgery (8, 9, 10). There is much speculation about the pathogenesis of endometriosis, but most studies support the theory that the disease is caused by the implantation of endometrial cells returned from the fallopian tubes into the abdominal cavity (11, 13).
One of the diagnostic methods of endometriosis is to use laparoscopy and see endometriotic areas and finally histological examination of these areas. Sur-geons and patients are more inclined to laparoscopic treatment rather than open surgery because it is a faster and less invasive procedure. Laparoscopic treatments include endometrioma aspiration, laparoscopic cystic-tomy, cyst drainage, and catheterization or laser, and even more radical treatments such as removal of part or all of the ovary and sometimes with uterine appendages (12, 13).
Although laparoscopy is the standard diagnostic method for endometriosis, possible complications in laparoscopic treatment include possible damage to other organs by laparoscopic devices, while the risk of infection, bleeding, postoperative illness, long-term hospitalization, ileus, deep vein thrombosis and other medical problems following laparotomy are common (14, 15, 16) . Laparoscopic treatment is also expensive and carries the risk of surgery (17).
Visual examination of the pelvis, as well as limitations such as the diagnosis of posterior pelvic, intestinal, and bladder involvement in endometriosis have led to the significant use of imaging techniques to treat and diagnose the disease. The advantages of using imaging techniques in the diagnosis of endometriosis include greater availability and acceptance for women and quick and cost-effective conclusions compared to surgical procedures. However, imaging methods depend on the skill of the operator and the extent of access to proper radiology facilities (18, 19).
Transvaginal ultrasound and MRI imaging are widely used in the diagnosis of deep lesions and recto-sigmoid involvement. Transvaginal ultrasound is useful in the diagnosis of ovarian endometrioma if the diameter is larger than 2 cm (18, 20). MRI and US ima-ging (including transabdominal, transvaginal, and transrectal) are the most common diagnostic methods for endometriosis (21, 22, 23). Transvaginal ultrasound is more useful in diagnosing endometriosis than other ovarian cysts (24, 25).
MRI imaging is used in the diagnosis of deep endometriosis lesions and is more effective than other methods in the diagnosis of small lesions (18, 20). Due to the importance of pelvic endometriosis, its comp-lications such as pain and infertility (26) and the limited number of studies on this disease in Iran, in this study, we have evaluated the diagnostic value of TVS (Tran-svaginal sonography) in the diagnosis of pelvic endometriosis compared with laparoscopic evaluation in patients referred to the imaging center of Imam Khomeini Hospital and Yas Hospital of Tehran in 2018.

Sampling Method and Sample Size

The study population was patients with pelvic endometriosis who were referred to the Imaging Center of Imam Khomeini Hospital and Yas Hospital of Tehran in 2018. The patients were suspected of endo-metriosis because of dysmenorrhea, dyspareunia, infer-tility, chronic pelvic pain, stable cyst or endometrioma, etc., and at the initial examination did not have a definitive diagnosis other than endometriosis to justify their symptoms. Exclusion criteria were dissatisfaction with the plan and patients with incomplete information.
In this diagnostic observational study, 69 patients with pelvic endometriosis who were referred to the Imaging Center of Imam Khomeini Hospital and Yas Hospital of Tehran in 2018 were randomly selected and entered into the study. All the obtained results were stored as typed ultrasound reports in patients' files to be used both for follow-up and clinical laparoscopic surgery (in the form of surgical description) and for study data. For each patient, the necessary information was collected and recorded from the TVS report in the patient file
The random selection method of data collection in this study was to review the records of patients, trans-vaginal ultrasound reports, and description of laparos-copic surgery and compare them in patients with endometriosis who underwent laparoscopic surgery. The mentioned information was extracted without mentioning the names of the patients and in a confi-dential manner, using an alternative numeric code for each patient and their results were evaluated as a group. TVS findings were gathered with the Siemens device and were compared with laparoscopic evaluation in the diagnosis of pelvic endometriosis and the sensitivity and specificity of TVS and the degree of agreement with laparoscopic results were determined.
The present article is part of the dissertation on "Evaluation of the diagnostic value of TVS (Trans-vaginal sonography) in the diagnosis of pelvic endo-metriosis in comparison with laparoscopic evaluation in patients referred to the Imaging Center of Imam Khomeini Hospital and Yas Hospital of Tehran in 2018 "In the specialized doctoral program in 2019 with ethics code 9511282001, which has been implemented with the support of Tehran University of Medical Sciences and Health Services.

Findings

The age of the patients in 29 cases (42%) was less than 35 years and in 40 cases (58%) was over 35 years. The pain was observed in 97.1%, infertility in 18.8% and uterine size above 80 mm in 59.4% of cases. Uterine myometrium echo pattern was homogeneous in 36.2%, heterogeneous in 63.8%, suggestive for adenomyosis in 34.8% and fibromatosis in 13% of cases. The position of the uterus on ultrasound was 88.4% anteverted and 7.2% retroverted. The remaining 4.4% had no uterus and underwent a hysterectomy, which did not fit into the above two categories.
In sonography, 34.8% had unilateral endometrium, 53.6% had bilateral endometrium, and 11.6% had no endometrium. In laparoscopy, 44.9% had unilateral endometrium, 43.5% had bilateral endometrium, and 11.6% had no endometrium.
In sonography, 36.2% of patients had a single DIE and 63.8% had multiple DIE. In laparoscopy, 33.3% of patients had single DIE and 50.7% had multiple DIE. 16% of cases were reported in laparoscopy without DIE nodules.
Frequency distribution of the site of involvement as DIE nodules in sonography was seen in 71% of patients, the distribution of which is as follows (Table 1).


Table 1. Comparison of the frequency of DIE based on the location of ultrasound and laparoscopy in patients

Laparoscopy Sonography  
Negative Positive Negative Positive  
25 (36.2%) 44 (63.8%) 20 (29%) 49 (71%) Nodule DIE
23 (33.3%) 25 (36.2%) Single DIE
35 (50.7%) 44 (63.8%) Multiple DIE
    Anterior compartment
67 (97.1%) 2 (2.9%) 69 (100%) 0 Bladder trigone
55 (79.7%) 14 (20.3%) 58 (84.1%) 11 (15.9%) Bladder base
61 (88.4%) 8 (11.6%) 68 (98.6%) 1 (1.4%) Bladder dome
69 (100%) 0 69 (100%) 0 Extra peritoneal part of bladder
59 (85.5%) 10 (14.5%) 67 (97.1%) 2 (2.9%) Distal ureter
    Posterior compartment
62 (89.9%) 7 (10.1%) 63 (91.3%) 6 (8.7%) Rectovaginal septum
36 (52.2%) 33 (47.8%) 40 (58%) 29 (42%) Uterosacral ligament
65 (94.2%) 4 (5.8%) 66 (95.7%) 3 (4.3%) Posterior vaginal fornix
52 (75.4%) 17 (24.6%) 49 (71%) 20 (29%) Torus uterinus
69 (100%) 0 69 (100%) 0 Posterior vaginal wall
63 (91.3%) 6 (8.7%) 63 (91.3%) 6 (8.7%) Lower rectum
61 (88.4%) 8 (11.6%) 56 (81.2%) 13 (18.8%) Upper rectum
29 (42%) 40 (58%) 51 (73.9%) 18 (26.1%) Rectosigmoid
68 (98.6%) 1 (1.4%) 69 (100%) 0 Sigmoid colon
    Other findings
56 (81.2%) 13 (18.8%) 66 (95.7%) 3 (4.3%) Peritoneal cyst

 

In the anterior compartment, 15.9% of the bladder base, 1.4% of the bladder dome, 2.9% of the distal ureter; In the posterior compartment, 8.7% of the rectovaginal septum, 42% of the uterosacral ligament, 4.3% of the posterior vaginal fornix, 29% of the torus uterinus, 8.7% of the lower rectum, 18.8% of the upper rectum, 26.1% of the rectosigmoid; in 4.3% of cases peritoneal cysts were seen. The frequency distribution of the site of involvement as DIE nodules in laparoscopy was reported in 63.8% of patients, which are as follows; In the anterior compartment 2.9% of the bladder trigone, 20.9% of the bladder base, 11.6% of the blad-der dome, 14.5% of the distal ureter; In the posterior compartment 10.1% rectovaginal septal involvement, 47.8% uterosacral ligament, 5.8% posterior vaginal fornix, 24.6% torus uterinus, 8.7% lower rectum, 11.6% upper rectum, 58% rectosigmoid, 1.4% of the sigmoid colon and 18.8% of peritoneal cysts were reported.
The mean size of endometriotic nodules varied from 12.7 to 25.6 mm in the patients examined based on ultrasound.
Regarding various findings (Table 2) in patients, the sensitivity and specificity of ultrasound in the diag-nosis of adhesion based on the sliding sign were:  in the anterior compartment 33.3% and 53%, and in the posterior compartment 7.1% and 92.7% (including 71.4% and 65.5% in retro cervix And 60% and 86.4% in posterior fundus). Also, the sensitivity and specificity of sonography in diagnosing unilateral endometrium was 83.3% and 90.2%, bilateral endometrium 93.3% and 76.9%, decreased left ovarian mobility 50% and 92.3%, fixed left ovarian mobility 88.5% and 74.4%, decreased right ovarian mobility 100% and 89.6%, fixed right ovarian mobility 84% and 72.7%, diffuse pelvic adhesion 90.2% and 55.6%, and Kissing ovaries 81.8% and 74.5%.
 

Table 2. Comparison of ultrasound and laparoscopic results of patients

Findings Sensitivity Specificity Compatibility rate
Adhesion in the anterior compartment 33.3 53 52.2
Adhesion in the posterior compartment 7.1 92.7 75.4
Adhesion of the recto cervix 71.4 65.5 66.7
Fundus adhesion 60 86.4 82.6
Unilateral endometrium 83.3 90.2 82.6
Bilateral endometrium 93.3 76.9 84.1
Decreased left ovarian mobility 50 92.3 89.6
Fixed mobility of left ovary 88.5 74.4 79.7
Decreased right ovarian mobility 100 89.6 89.6
Fixed mobility of right ovary 84 72.7 76.8
Pelvic adhesions  (frozen pelvic) 90.2 55.6 81.2
Kissing ovary 81.8 74.5 76.8

 

Ultrasonic and laparoscopic consistency in the diagnosis of adhesions is as follows, in the anterior compartment 52.2%, in the posterior compartment 75.4% (including 66.7% in the retro cervix, 82.6% in posterior fundus), unilateral endometrium 82.6%, bilateral endometrium 84.1%, decreased left ovarian mobility 89.6%, fixed left ovarian mobility 79.7%, decreased right ovarian mobility 89.6%, fixed right ovarian mobility 76.8%, diffuse pelvic adhesion 81.2% and 76.8% was related to kissing ovaries.
In this study, the sensitivity and specificity of ultra-sound in the case of DIE detection (Table 3) as nodules were 88.6% and 60%, single involvement 52.2% and 71.7%, multiple involvement 54.3% and 76.5%, anterior compartment involvement including bladder base 64.3% and 96.4%, bladder dome 87.5% and 100%, distal ureter 10% and 98.3% and posterior compartment involvement including rectovaginal septum 42.9% and 95.2%, uterosacral ligament 75.8% and 88.9%, posterior vaginal fornix 25% and 96.9%, Torus uterinus 94.1% and 92.3%, Lower rectum 50% and 95.2%, Upper rectum 62.5% and 86.9%, Rectosigmoid 42.5% and 96.6%, accompanying findings such as peritoneal cyst 23.1% and 100% and tubal involvement were 43.8% and 67.6%. Ultrasound has indefinite sensitivity in the diagnosis of bladder trigone and sigmoid colon involvement but has 100% specificity.

 

 Table 3. Comparison of involvement site in ultrasound and laparoscopy of patients

Site of involvement Sensitivity Specificity Compatibility rate
Presence of DIE nodule 88.6 60 78.3
Single DIE nodule 52.2 71.7 65.2
Multiple DIE nodules 54.3 76.5 65.2
Bladder trigone --- 100 97.1
Bladder base 64.3 96.4 89.9
Bladder dome 87.5 100 89.9
Distal ureter 10 98.3 85.5
Rectovaginal septum 42.9 95.2 89.9
Uterosacral ligament 75.8 88.9 82.6
Posterior vaginal fornix 25 96.9 92.7
Torus uterinus 94.1 92.3 92.7
Lower rectum 50 95.2 91.3
Upper rectum 62.5 86.9 84.1
Rectosigmoid 42.5 96.6 65.2
Sigmoid colon --- 100 98.6
Peritoneal cyst 23.1 100 85.5
Tubal involvement 43.8 67.6 56.5

 

 

Ultrasonic and laparoscopic compatibility of DIE detection as nodules were 78.3%, single involvement 65.2%, multiple involvement 65.2%, anterior compartment involvement including bladder trigone 97.1%, bladder base 89.9%, bladder dome 89.9%, distal ureter 85.5 %, Posterior compartment involvement including rectovaginal septum 89.9%, uterosacral ligament 82.6%, posterior vaginal fornix 92.7%, torus uterinus 92.7%, lower rectum 91.3%, upper rectum 84.1%, rectosigmoid 65.2%, sigmoid colon 98.6%. Accompanying findings such as peritoneal cyst was 85.5% and tubular involvement was 56.5%.


 

Results
 

Endometriosis is an important cause of pelvic pain and infertility in women. Ultrasound imaging and MRI are the most common diagnostic methods for endometriosis. Ultrasound is a suitable modality for assessing the extent and spread of involvement in endometriosis patients due to its high accuracy, low cost and availability. Transvaginal ultrasound is useful in diagnosing ovarian endometrioma if it is larger than 2 cm in diameter and is more useful in diagnosing endometriosis than other ovarian cysts. Therefore, in this study, we investigated the diagnostic value of TVS in the diagnosis of pelvic endometriosis in comparison with laparoscopic evalua-tion in patients who were referred to the Imaging Center of Imam Khomeini Hospital and Yas Hospital of Tehran in 2018.
In this study, the sensitivity and specificity of sonography in the case of DIE detection as nodules were 88.6% and 60%, single involvement detection 52.2% and 71.7%, multiple involvement detection 54.3% and 76.5%, anterior compartment involvement including bladder base 64.3% and 96.4%, bladder dome 87.5% and 100%, distal ureter 10% and 98.3% and posterior compartment involvement including rectovaginal septum 42.9% and 95.2%, uterosacral ligament 75.8% and 88.9%, posterior vaginal fornix 25% and 96.9%, Torus uterinus 94.1% and 92.3%, lower rectum 50% and 95.2%, upper rectum 62.5% and 86.9%, rectosigmoid 42.5% and 96.6% and associated findings such as peritoneal cysts were 23.1% and 100% and tubal involvement 43.8% and 67.6%, respectively. Ultrasound is indeterminate in the diagnosis of bladder trigone and sigmoid colon involvement but has 100% specificity.

 
 

 

Discussion

 

Ultrasonic and laparoscopic compatibility of DIE detection as nodules was 78.3%, follows by single involvement detection 65.2%, multiple involvement detection 65.2%, anterior compartment involvement, including bladder trigone 97.1%, bladder base 89.9%, bladder dome 89.9%, distal ureter 85.5 %, posterior compartment involvement including rectovaginal septum 89.9%, uterosacral ligament 82.6%, posterior vaginal fornix 92.7%, torus uterinus 92.7%, lower rectum 91.3%, upper rectum 84.1%, rectosigmoid 65.2%,  peritoneal cyst 85.5% and tubular involvement 56.5%.
In a study by Tadros et al. (2016), the role of transvaginal ultrasound in the study of superficial and deep endometriosis was investigated. Sensitivity, specificity and overall accuracy of transvaginal ultra-sound were calculated to be 88%, 33% and 76%, respectively. Therefore, MRI imaging was a very useful method in determining the rate of endometriosis, which is in line with the results of our research. In a study, Said et al. (2014) evaluated the possibility of predicting endometriosis by transvaginal ultrasound in 125 women with normal ovarian size and mean age of 29 (19 to 46 years) and the sensitivity, specificity, NPV, PPV and diagnostic accuracy of endometriosis diagnosis were 85.3%, 80.7%, 84.1%, 82.1% and 83.2%, respectively. They stated that transvaginal ultrasound is a useful method in predicting endometriosis, which is consistent with the findings of our study. In the study by Abrao et al. (2007), they compared the results of transvaginal ultrasound and MRI imaging (T1 and T2) in 104 patients for the diagnosis of endometriosis (rectosigmoid). Sensitivity, specificity and accuracy of the test in the diagnosis of endometriosis on transvaginal ultrasound were 98.1%, 100% and 99%, respectively. Also, the sensitivity, specificity and accuracy of the test in the diagnosis of rectosigmoid on transvaginal ultrasound were 95.1%, 98.4% and 97%. Compared to MRI, transvaginal ultrasound was slightly better in the diagnosis of endometriosis, thus it confirms our findings. Ghezzi et al. (2005) examined 722 premeno-pausal women suspected of having pelvic endomet-riosis. Ultrasound was performed before surgery and the diagnostic value of ultrasound in the diagnosis of ovarian cysts and endometriosis was evaluated. According to the results of the ultrasound, which showed endometriosis, 309 patients underwent laparoscopy. The results showed that the diagnosis of ovarian cyst on ultrasound was directly and significantly related to endometriosis and is one of the symptoms of this disease that is consistent with the results of our study. In a study conducted by Holland et al. in the UK and published in 2013, 198 women underwent TVS ultrasound and it was determined that the sensitivity and specificity for endometriosis lesions of the bladder was 100% , for ovaries 84% and 95.6% and the rectum is 33% and 98.9%, which is in line with the results of our research.
Therefore, due to the fact that laparoscopy is a surgery and imaging methods have high accuracy for diagnosing endometriosis, the need for laparoscopy to diagnose the disease is eliminated in a high percentage of patients.

 

 
Conclusion

In general, it is inferred that the highest diagnostic sensitivity of TVS in cases of pelvic endometriosis is related to the involvement of the torus uterinus and bladder dome, and its highest specificity is related to the involvement of the bladder, sigmoid colon and peritoneal cyst, and in case of bladder trigone and sigmoid colon involvement there is the most consistency of TVS with laparoscopic evaluation. Based on laparoscopic findings, involvement of some parts of the abdomen, including the diaphragm, appe-ndix, and serosal surfaces of the intestine, is freq-uently reported which ultrasound sensitivity is not optimal for their diagnosis and multi-modal examination and integration of MRI and ultrasound findings is needed to increase sensitivity and specificity of Imaging.
However, in the end, multicenter studies with higher sample sizes and comparison with the results of other diagnostic methods are recommended to achieve more documented results.


 

Acknowledgments

 

The present article is part of the dissertation on "Evaluation of the diagnostic value of TVS (Trans-vaginal sonography) in the diagnosis of pelvic endo-metriosis in comparison with laparoscopic evaluation in patients referred to the Imaging Center of Imam Khomeini Hospital and Yas Hospital of Tehran in 2018 "In the specialized doctoral program in 2019 with ethics code 9511282001, which has been implemented with the support of Tehran University of Medical Sciences and Health Services.

 

Conflicts of Interest

The authors declared no conflict of interest.

 

 
1. Elevated serum lipoprotein(a) levels in young women with endometriosis.Metabolism. 1997 Jul;46(7):735-9. [DOI:10.1016/S0026-0495(97)90115-3]
2. Pretta S، Remorgida V، Abbamonte LH، Anserini P،Ragni N، Del Sette M، et al. Atherosclerosis in women with endometriosis. Eur J Obstet Gynecol Reprod Biol 2007;132:226-31. [DOI:10.1016/j.ejogrb.2006.04.015] [PMID]
3. Szczepanska M، Kozlik J، Skrzypczak J، Mikolajczyk M. Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril. 2003;79: 1288-93. [DOI:10.1016/S0015-0282(03)00266-8]
4. Van Langendonckt A، Casanas-Roux F، Donnez J. Oxidative stress and peritoneal endometriosis. Fertil Steril 2002;77:861-70. [DOI:10.1016/S0015-0282(02)02959-X]
5. Holland TK, Cutner A, Saridogan E, Mavrelos D, Pateman K, Jurkovic D. Ultrasound mapping of pelvic endometriosis: does the location and number of lesions affect the diagnostic accuracy? A multicentre diagnostic accuracy study. BMC Womens Health. 2013;13:43. [DOI:10.1186/1472-6874-13-43] [PMID] [PMCID]
6. Vigano P, Parazzini F, Somigliana E, Vercellini P. Endometriosis: epidemiology and aetiological factors. Best practice & research Clinical obstetrics & gynaecology. 2004 Apr 30;18(2):177-200. [DOI:10.1016/j.bpobgyn.2004.01.007] [PMID]
7. Chapron C, Vercellini P, Barakat H, Vieira M, Dubuisson JB. Management of ovarian endometriomas. Human reproduction update. 2002 Nov 1;8(6):591-7. [DOI:10.1093/humupd/8.6.591] [PMID]
8. Salehpour S, Zhaam H, Hakimifard M, Khalili L, Azar Gashb Y. Evaluation of Diagnostic Visual Findings at Laparoscopy in Endometriosis. International Journal of Fertility and Sterility. 2007;1(3):123-6
9. Redwine DB, Koning M, Sharpe DR. Laparoscopically assisted transvaginal segmental resection of the rectosigmoid colon for endometriosis. Fertility and sterility. 1996 Jan 31;65(1):193-7. [DOI:10.1016/S0015-0282(16)58051-0]
10. Yuen PM, Yu KM, Yip SK, Lau WC, Rogers MS, Chang A. A randomized prospective study of laparoscopy and laparotomy in the management of benign ovarian masses. American journal of obstetrics and gynecology. 1997 Jul 31;177(1):109-14. [DOI:10.1016/S0002-9378(97)70447-2]
11. Adamson GD, Subak LL, Pasta DJ, Hurd SJ, von Franque O, Rodriguez BD. Comparison of CO 2 laser laparoscopy with laparotomy for treatment of endometriomata. Fertility and sterility. 1992 May 31;57(5):965-73. [DOI:10.1016/S0015-0282(16)55010-9]
12. Sawada T, Ohara S, Kawakami S. Laparoscopic surgery vs. laparotomy management for infertile patients with ovarian endometrioma. Gynaecological Endoscopy. 1999 Feb 1;8(1):17-9. [DOI:10.1046/j.1365-2508.1999.00235.x]
13. Nisenblat V, Bossuyt PM, Farquhar C, Johnson N, Hull ML. Imaging modalities for the non-invasive diagnosis of endometriosis. The Cochrane Library. 2016 Jan 1. [DOI:10.1002/14651858.CD009591.pub2] [PMID] [PMCID]
14. Brosens I, Puttemans P, Campo R, Gordts S, Kinkel K. Diagnosis of endometriosis: pelvic endoscopy and imaging techniques. Best Practice & Research Clinical Obstetrics & Gynaecology. 2004 Apr 30;18(2):285-303. [DOI:10.1016/j.bpobgyn.2004.03.002] [PMID]
15. Moore J, Copley S, Morris J, Lindsell D, Golding S, Kennedy S. A systematic review of the accuracy of ultrasound in the diagnosis of endometriosis. Ultrasound in obstetrics & gynecology. 2002 Dec 1;20(6):630-4. [DOI:10.1046/j.1469-0705.2002.00862.x] [PMID]
16. Kinkel K, Frei KA, Balleyguier C, Chapron C. Diagnosis of endometriosis with imaging: a review. European radiology. 2006 Feb 1;16(2):285-98. [DOI:10.1007/s00330-005-2882-y] [PMID]
17. Abrao MS, Gonçalves MO, Dias Jr JA, Podgaec S, Chamie LP, Blasbalg R. Comparison between clinical examination, transvaginal sonography and magnetic resonance imaging for the diagnosis of deep endometriosis. Human Reproduction. 2007 Oct 18;22(12):3092-7. [DOI:10.1093/humrep/dem187] [PMID]
18. Alborzi S, Zarei A, Alborzi S, Alborzi M. Management of ovarian endometrioma. Clinical obstetrics and gynecology. 2006 Sep 1;49(3):480-91. [DOI:10.1097/00003081-200609000-00008] [PMID]
19. Ghezzi F, Raio L, Cromi A, Duwe DG, Beretta P, Buttarelli M, Mueller MD. "Kissing ovaries": a sonographic sign of moderate to severe endometriosis. Fertility and sterility. 2005 Jan 31;83(1):143-7. [DOI:10.1016/j.fertnstert.2004.05.094] [PMID]
20. Rauch GM, Kaur H, Choi H, Ernst RD, Klopp AH, Boonsirikamchai P, Westin SN, Marcal LP. Optimization of MR imaging for pretreatment evaluation of patients with endometrial and cervical cancer. Radiographics. 2014 Jul 14;34(4):1082-98. [DOI:10.1148/rg.344140001] [PMID] [PMCID]
21. Said TH, Azzam AZ. Prediction of endometriosis by transvaginal ultrasound in reproductive-age women with normal ovarian size. Middle East Fertility Society Journal. 2014 Sep 30;19(3):197-207. [DOI:10.1016/j.mefs.2013.11.003]
22. Sehgal V, Delproposto Z, Haacke EM, Tong KA, Wycliffe N, Kido DK, Xu Y, Neelavalli J, Haddar D, Reichenbach JR. Clinical applications of neuroimaging with susceptibility-weighted imaging. Journal of Magnetic Resonance Imaging. 2005 Oct 1;22(4):439-50. [DOI:10.1002/jmri.20404] [PMID]
23. Takeuchi M, Matsuzaki K, Nishitani H. Susceptibility-weighted MRI of endometrioma: preliminary results. American Journal of Roentgenology. 2008 Nov;191(5):1366-70. [DOI:10.2214/AJR.07.3974] [PMID]
24. Tadros MY, Keriakos NN. Diffusion MRI versus ultrasound in superficial and deep endometriosis. The Egyptian Journal of Radiology and Nuclear Medicine. 2016 Dec 31;47(4):1765-71. [DOI:10.1016/j.ejrnm.2016.07.011]
25. Endometriosis - morphology, clinical presentations and molecular pathology. J Lab Physicians. 2010 Jan;2(1):1-9.
26. Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol. 2014;10(5):261-75. [DOI:10.1038/nrendo.2013.255] [PMID]
27. Rahmani M, Moradi B, Gity M, Chavoshi M, Hantoushzadeh S, Kazemi Aski S, et al . Clinical characteristics, CT features and perinatal outcome of COVID-19 pneumonia in pregnant women and comparison with non-pregnant women. J Obstet Gynecol Cancer Res. 2021; 6 (2) :72-80 [DOI:10.30699/jogcr.6.2.72]