Detorsion or Adnexectomy for Adnexal Torsion and MRI Assessment for Necrosis

Abstract

Objective: Adnexal torsion (AT) is an ischemic process that evolves over time till necrosis. Unfortunately, there are no investigations or intraoperative findings to predict adnexal necrosis. The question of this study is, “Can MRI detect necrotic or non-necrotic adnexa?” Detorsion of viable twisted adnexa can preserve a functioning ovary. Design: Prospective study. Patients and Methods: Thirteen patients of suspected AT on the basis of clinical, ultrasound, and color Doppler were immediately transferred for magnetic resonance imaging (MRI) to be done and then emergency laparoscopy was planned. After laparoscopic confirmation of AT, the first step was to untwist the adnexa and assess the potential for tissue recovery; then, adnexectomy was carried out only when the adnexa was necrotic and there was no recovery after detorsion. Results: MRI suspected hemorrhagic infarction in only one case. Adnexectomy was performed for the same case of suspected MRI necrosis. Follow up of the 12 detorsion cases revealed normal ovarian functions. The main limitation of this study is the low number of studied patients due to relative rarity of AT. Conclusion: MRI may be a promising tool to detect viability adnexa, and the decision of detorsion operation can be done to preserve ovarian function. Many studies still need to support this conclusion. (J GYNECOL SURG 31:336)

Introduction

Adnexal torsion (AT) is a gynecologic emergency, as it is an ischemic process that evolves over time till necrosis.¹ AT is the rotation of at least one turn of the ovaries, adnexa, or the fallopian tube around the line of the tubo-ovarian ligament and the infundibulopelvic ligament.² Twisting of the ovary on its pedicle causes lymphatic and venous stasis and, consequently, ovarian edema, followed by ischemia and necrosis when left untwisted. No specific clinical manifestation or any sensitive biochemical marker is available for diagnosing AT or ischemia.³ Triage is necessary to identify which patients should be given priority care to reduce excessive delay of treatment.⁴

For ∼100 years after its initial description in the American literature by J. Bland Sutton, AT was treated by performing a salpingo-oophorectomy without untwisting the adnexa to avoid potential thromboembolism from ovarian vein thrombosis.⁵ However, a significant association between thromboembolism and detorsion of an ischemic pedicle has never been established.⁶ Mage et al. proved that detorsion and preservation of adnexa is an alternative mode of treatment and ever since it has become the method of approach.⁷ Many reports describe minimally invasive laparoscopic detorsion with preservation of the ovary.^8–10

About 23% to 66% of AT were correctly diagnosed before surgery.^10,11 Warner et al. warned that the association of an adnexal mass detected by sonography and pain should prompt consideration of AT as a diagnosis.³ The unilateral pain at vaginal touch would tend to indicate AT.⁹ Ultrasound alone is an inadequate diagnostic tool.^12,13 Doppler can only diagnose interruptions of the arterial flow and cannot diagnose venous flow interruptions, which often precede arterial interruptions, so a normal Doppler result cannot exclude the diagnosis of AT.¹² Magnetic resonance imaging (MRI) can provide accurate information about hemorrhage, fat, and collagen and it is able to identify different types of tissue contained in pelvic masses.^14,15 MRI may be more helpful than CT in detecting a thickened tube and hemorrhagic infarction by better detection of eccentric smooth wall thickening in a cystic ovarian mass converging on the thickened tube, lack of contrast enhancement of the internal solid component or the thickened wall of a twisted ovarian mass, hemorrhage within the tube or twisted ovarian mass, and hemoperitoneum.^15–18

The aim of this study is to evaluate the preoperative MRI findings suggesting ovarian necrosis to detect which ovary can be detorsred and kept in place to preserve the functioning ovary or should be removed to avoid the possible complications of necrotic nonfunctioning adnexa.

Patients and Methods

This is a prospective study of 13 patients who underwent operative laparoscopy for AT. This study was conducted in Zagazig University Hospital, Zagazig, Egypt, over a period between April 2012 and April 2014. The study was reviewed and approved by the institutional review board. Written informed consents were obtained from cases of AT before entry into the study.

The patients with AT were suspected on the basis of signs and symptoms; then, an immediate ultrasound with color Doppler was performed as the investigation of choice. All cases with suspected twisted adnexa were immediately transferred for an MRI to be done. Emergency surgical laparoscopy was planned after high suspicion of AT. Laparoscopy confirmed diagnosis followed by detorsion for non-necrotic adnexa or excision of necrotic adnexa.

All cases with less than a 360° rotation of the pedicle, malignant ovarian tumors, and pelvic adhesions were excluded. Cases were also excluded if laparoscopy delayed more than 3 hours from hospital admission.

AT is suspected clinically

Patients with AT usually complained of a sudden onset of intense lower abdominal pain. Pain may be associated with nausea and vomiting and sometimes fever. The clinical examination provoked unilateral pain, which may or may not be associated with signs of peritoneal irritation (abdominal tenderness and guarding). A latero-uterine mass may be found during clinical examination.⁹

Sonographic and Doppler findings of torsion

Initially, this should be abdominal with the bladder full in order not to miss an adnexal mass located high in the abdomen; then, if possible, transvaginal with the bladder empty for optimum assessment of the adnexa in a standardized fashion.¹⁷ Pregnant and virginal patients and those immediately postpartum were examined transabdominally only. Standard transabdominal or transvaginal two-dimensional color Doppler sonography of the patients was conducted with Acuson Sequoia and Aspen scanners (Siemens Medical Solutions USA, Inc.). Examinations were conducted with 2- to 5-MHz curved array probes and 4- to 8-MHz transvaginal probes. Sonographic findings of torsion are ovarian enlargement, massive ovarian edema, and free fluid in cul-de-sac.^14,17 Follicles positioned around the periphery of the ovary are often identified as well, an appearance believed to result from peripheral displacement as a result of stromal edema.¹⁷ Hyperechoic and hypoechoic areas may be seen, which correspond to hemorrhage and edema, respectively.¹⁶ For Doppler assessment, an appropriate low-velocity pulse repetition frequency setting was used for intraovarian flow, with gradually decreasing pulse repetition frequency down to 500 Hz, especially when flow was difficult to detect. Abnormal flow on color Doppler of twisted pedicle classically presents as a rounded hyperechoic mass with central hypoechoic vessels in a target-like configuration.¹² There may also be a beak-like configuration of the vessels at one margin of the mass, resulting from twisting of the vascular structures.¹²

Magnetic resonance imaging

MRI was performed using a 1.5 T MR imaging system (Intera Achieva 1.5T Pulsar; Philips Medical Systems) with a phased-array body coil to allow whole pelvic coverage. The parallel imaging at a section thickness of 5 mm, with a 2 mm intersection gap and a 28×28 cm field of view, was used in the transverse planar in all images. Non-fat suppressed T1- and T2-weighted spin echo were obtained. All patients had fast-spin-echo T2-weighted (TR, 4500–5600; TE, 96–132) and spin-echo T1-weighted (TR, 440–680; TE, 10–13) sequences in at least one plane. The MRI data analysis was done by both radiologists, and one report was approved by both of them (M.S.H. and M.A.H.).

Features of torsion that have been reported on MRI include pelvic free fluid, deviation of the uterus to the side of the twist, engorged vessels on the twisted side, and fallopian tube thickening.^18,19 The enlarged edematous ovary with peripheral follicles is best seen on fast-spin-echo T2-weighted MRI without fat saturation.¹⁵ In cases of hemorrhagic infarct, a few characteristic findings can be seen, including a beaked protrusion at the periphery of the affected ovary due to hematoma and absence of enhancement.¹⁷ The presence of hematoma is highly associated with infarction and necrosis of the involved ovary. Hemorrhage is best detected on T1-weighted images with fat saturation.¹⁶ A T1-hyperintense rim of a hematoma is seen within an enlarged ovary; heterogeneous minimal or absent enhancement indicates the evolution of ovarian torsion from ischemia to infarction.¹⁸

After radiologic diagnosis, the patient was taken to the operating theater (OR) on an emergency basis. Laparoscopy was the initial mode of management followed by laparotomy if required. To reduce subjective operator bias, surgery was performed by the same gynecologic surgeon (M.F.S.), who was blind about the MRI report for the presence or absence of necrosis.

The first step in the operation was to confirm the diagnosis and specify which organs (tube, ovary, or both) were involved in the torsion as well as in the number of turns. Subsequently, the first action was to untwist the adnexa and assess the potential for recovery of the tissues. Patients were then assigned to four groups according to a classification previously published by Karayalçın et al.:⁸

• Grade 1 (no evidence of ischemia): Slightly discolored ovary, which promptly reverted to normal color after detorsion.

• Grade 2 (mild ischemic lesions with recovery within 10 minutes after detorsion): Dark red to brown ovary, which became hyperemic with multiple pin-point petechiae after detorsion.

• Grade 3 (marked ischemia adnexa with recovery): Brown to black, grossly enlarged ovary with hematoma with partial improvement in color within 10 minutes, small pin-point oozing after detorsion, and hematoma evacuation.

• Grade 4 (marked ischemia adnexa without recovery) Completely black, grossly enlarged ovary with hematoma and no improvement in color after detorsion and hematoma evacuation for more than 10 minutes.

Detorsion was done whenever ischemic lesions were minimal and/or there were obvious signs of recovery. The ovaries underwent either simple detorsion or detorsion with evacuation of hematoma or cystectomy if there were ovarian cysts. None of the ovaries was fixed.

Technical procedure

Laparoscopy was performed in all patients using three puncture techniques. A Veress needle was placed via a vertical incision into the umbilicus, and the pneumoperitoneum was formed with a pressure of 12 to 15 mm Hg to place a 10-mm trocar. Trocars (5 mm) were placed in left and right iliac spines. Initially, the whole peritoneal cavity was inspected as a whole to confirm the diagnosis, exclude malignancy, and inspect the contra-lateral ovary.

When pedicle torsion of an adnexal cyst was confirmed, detorsion was slowly and gently performed using a non-traumatic vascular clamp. To untwist the adnexa, blunt manipulation was preferred to grasping, thus avoiding additional damage and bleeding. Using an atraumatic forceps or a 5-mm probe, the twisted organs were moved slowly and gently according to “Kustner's law” (the left side the pedicle of the twisted organs was rotated in a clockwise direction, whereas it would rotate in a counterclockwise direction on the right side).¹⁹ The cyst was punctured to aspirate cystic fluid before detorsion if it was large. For severe ischemia, when the color is dark, cysts may be punctured to decrease the tension and are soaked in saline for 10 minutes to observe whether the blood circulation recovers.²⁰ Detorsion remains feasible if circulation recovers within 10 minutes. If not, oophorectomy or salpingectomy is recommended. In cases with ovarian cysts, after stabilizing the ovary, a superficial incision was made with diathermy on the anti-mesenteric border. The incision was gently enlarged to separate the cyst from the surrounding ovarian tissue. Hemostasis was achieved, and the cyst was retrieved through a custom-made bag through the 10 mm umbilical port after changing the camera to another port site.

Follow-up gray-scale and color Doppler ultrasound were performed a week, 1 month, and 3 month post-laparoscopy for patients who were conservatively managed to determine the outcome of the adnexa. Patient follow-up was conducted at our outpatient clinic by the same surgeon (M.F.S.).

The demographic data, including age, marital status, and previous medical history, were noted. The time of onset of symptoms, time of admission to hospital, and ultrasonographic, color Doppler, and MRI findings were reported. All the patients underwent laparoscopic management. The time interval between hospital admission and surgery, type of intervention, and operative findings were recorded. In addition, torsion of ovary was graded by laparoscopy into four grades. Follow-up data obtained included success of detorsion in the torsed ovary resuming its normal perfusion and reproductive activity.

Statistical analysis

All variables were presented as the numbers or mean values±standard deviations, and p<0.05 was considered to indicate statistically significant differences. All statistical calculations were performed using SPSS 22 (SPSS version 22).

Results

The study includes 13 patients with a mean age of 22.7±10.5 years (a range of 13–41 years): 9 patients (69.2%) were married, and 4 (30.8%) were unmarried. All presented with unilateral lower abdomen pain, some with nausea (11 cases of 84.6%), vomiting in 9 cases (69.2%), and fever in only 3 cases (23.4%). Abdominal tenderness and guarding were detected in 10 cases (76.9%). Leukocytosis (WBCs≥11,000) was also found in eight cases (61.5%). The mean time from onset of symptoms to hospital admission is 16.6±4.5 hours, and the mean time from hospital admission to operation is 2.1±0.6. During surgery, Adnexectomy has been done for only 1 case (7.7%) and the preservation of adnexa with detorsion procedures has been done in 12 cases (92.3%). All patients underwent preoperative ultrasonography and color Doppler assessments. A pelvic mass was detected in 12 cases (92.3%), distended fallopian tube in 9 cases (69.2%), and free pelvic fluid in 12 cases (92.3%). The mean diameter of torsed mass was 11.3±3.6 cm, while the mean diameter of the contralateral ovary was 3.2±1.9 cm. In 2 (15.4%) patients, ovarian blood flow by color Doppler was found to be normal; while in 11 (84.6%) patients, it was pathological. Arterial and venous flow was absent in seven cases (53.8%) and arterial flow was present; however, venous flow was absent in four cases (30.8%). Doppler study also showed a ring sign in nine cases (69.2%) only (Table 1).

Table 1.

Demographic and Clinical Data (for Total 13 Cases)

Data	Values
Age (years, mean±SD)	22.7±10.5
Married (n, %)	9 (69.2)
Unmarried (n, %)	4 (30.8)
Symptoms and signs
Nausea (n, %)	11 (84.6)
Vomiting (n, %)	9 (69.2)
Fever with temperature ≥38°C (n, %)	3 (23.4)
Abdominal tenderness and guarding (n, %)	10 (76.9)
Leukocytosis (WBCs≥11,000)	8 (61.5)
Time from hospital admission to operation (h, mean±SD)	2.1±0.6
Time from onset of symptoms to hospital admission (h, mean±SD)	16.6±4.5
Detrorsion conservative surgery (n, %)	12 (92.3)
Adnexectomy (n, %)	1 (7.7)
Ultrasonographic findings
Diameter of torsed mass (cm, mean±SD)	11.3±3.6
Diameter of contralateral ovary (cm, mean±SD)	3.2±1.9
Presence of adnexal cysts (n, %)	12 (92.3)
Distended fallopian tube (n, %)	9 (69.2)
Free pelvic fluid (n, %)	12 (92.3)
Doppler findings (n, %)
Arterial and venous flow absent	7 (53.8)
Arterial flow present but venous flow absent	4 (30.8)
Normal flow	2 (15.4)
Presence of ring sign	9 (69.2)
MRI findings (n, %)
Fallopian tube thickening	13 (100)
Wall thickening of torsed ovarian lesion	8 (61.5)
Uterine deviation to the twisted side	5 (38.4)
Free pelvic fluid	12 (92.3)
Adnexa torsion with hemorrhagic infarction	1 (7.7)
Surgical findings (n, %)
Ovarian torsion only	1 (7.7)
Ovarian along with tubal torsion	12 (92.3)
Grades after detorsion (n, %)
Grade 1	3 (23.1)
Grade 2	4 (30.8)
Grade 3	5 (38.4)
Grade 4	1 (7.7)

MRI, magnetic resonance imaging.

By MRI, fallopian tube thickening was detected in all 13 studied cases (100%), wall thickening of torsed ovarian lesion in 8 cases (61.5%), uterine deviation to the twisted side in 5 cases (38.4%), and free pelvic fluid in 12 cases (92.3%). The MRI showed hemorrhagic infarctions in 1 (7.7%) case (Table 1).

Laparoscopic surgery succeeded without conversion to laparotomy or thromboembolism in all patients. All were discharged home within 2 days after surgery. During laparoscopy, the torsion involved the ovarian tissue only in 1 case (7.7%) and ovarian along with tubal torsion was detected in 12 cases (92.3%). AT had been rotated from completed one to five times. After surgical detorsion, there were three cases (23.1%) as grade 1 torsion, four cases (30.8%) as grade 2, five cases (38.4%) as grade 3, and finally one case (7.7%) as grade 4 that underwent adnexectomy (Table 1).

Table 2 summarizes MRI findings in the case with suspected hemorrhagic infarctions and cases without infarction. Fallopian tube thickening, smooth wall thickening of torsed ovarian cystic lesion, and free pelvic fluid were observed in the case (100%) of suspected hemorrhagic infarction. Fallopian tube thickening was detected in all cases (100%) without hemorrhagic infarction. Smooth wall thickening of torsed ovarian cystic lesion was detected in only 6 of 12 cases (50%) without suspected hemorrhagic infarction, and free pelvic fluid was detected in 10 of the 12 cases (83.3%) without infarction. Uterine deviation to the twisted side was observed in the case (100%) with infarction and in four cases (33.3%) without infarction. Table 2 also shows a significantly (p≤0.5) higher quantitative non-fat suppressed T1-weighted spin-echo of torsed mass with hemorrhagic infarction compared with cases without infarction; however, quantitative non-fat suppressed T2-weighted spin-echo does not differ significantly between hemorrhagic infarction and without infarction AT cases. MRI suggested adnexal necrosis in the same case that was proved surgically and histopathologically with necrosis.

Table 2.

MRI Findings in Patients With and Without Hemorrhagic Infarctions

	Without hemorrhagic infarction	With hemorrhagic infarction
MRI findings	N=12 cases	N=1 case
Fallopian tube thickening (n, %)	12/12 (100)	1/1 (100)
Wall thickening of torsed ovarian lesion (n, %)	6/12 (50)	1/1 (100)
Uterine deviation to the twisted side (n, %)	4/12 (33.3)	1/1 (100)
Free pelvic fluid (n, %)	10/12 (83.3)	1/1 (100)
Quantitative non-fat suppressed T1-weighted spin-echo (mean±SD)	1.23±0.21^a	1.96±0.59
Quantitative non-fat suppressed T2-weighted spin-echo (mean±SD)	0.89±0.30	0.80±0.33

Means significant (p≤0.5).

Follow-up gray-scale and Doppler sonography were performed for all 12 patients with preserved ovarian tissue in the first week, the first and the third months after laparoscopic surgery. The ipsilateral ovarian size, follicular development, and ovary blood flow appeared normal in all cases 1 and 3 months after surgery. The patients who wanted to have children (seven cases) conceived naturally within 3 to 10 months after surgery.

Discussion

With unrelieved torsion, adnexal edema may evolve toward hemorrhagic infarction and necrosis. Early detection before hemorrhagic infarction is essential to do the detorsion procedure.¹⁸ Torsion occurs more commonly in young women with the greatest incidence in the 20- to 30 year age group.¹⁹ Mage et al. performed oophorectomy if the ovary appeared gangrenous at operation, and detorsion alone if the ovary did not appear gangrenous.⁷ The old concept of the risk of systemic inflammatory response syndrome after detorsion in necrotic adnexa due to reperfusion injury has also been changed to that after detorsion; even if ovarian masses look hemorrhagic and friable, ovarian function has been found to be preserved.¹⁹ The ability to retain viability despite prolonged ischemia indicates that complete arterial obstruction does not usually occur, and some blood supply can still be obtained from either the ovarian or uterine arteries and the ischemic hemorrhagic appearance of the adnexa is due to venous and lymphatic stasis rather than gangrene.¹¹ Oelsner et al. reported that 40 patients with ischemic adnexa encountered at surgery were managed by unwinding of the adnexa. Three patients were lost to follow-up. A normal sized ovary, with follicular development, was demonstrated sonographically in 35 of 37 treated patients.¹¹ A prospective study was conducted by Karayalçın et al. on 36 patients who underwent operations for AT via laparoscopy. Laparoscopic conservative treatment was performed in 34 patients. Postoperative ultrasonographic examinations confirmed normal ovarian morphology and Doppler blood flow in all patients with no recurrence.⁸ Oelsner et al. strongly supported the conservative approach for management of the twisted ischemic adnexa whenever fertility was desired, as ovarian function was apparently maintained in 91.3% of patients and in the 8.7% of patients whose ovaries were irreversibly damaged by ischemia.¹¹ Management of pedicle torsion with adnexal cysts is safe and reliable, cysts may be punctured to decrease the tension, and conservative surgery remains feasible if circulation recovers within 10 minutes. If not, oophorectomy or salpingectomy is recommended.²⁰

Unfortunately, there is no preoperative way to predict which ovaries have been too severely injured to recover and further research is necessary to develop methods of determining the viability of the ovary. Meanwhile, MRI is substantial in terms of depiction of hemorrhagic infarction after ovarian torsion because of its high sensitivity for hemorrhage, as the signal intensity of hemorrhage depends on the chemical state of iron (ferrous or ferric) in the hemoglobin molecule and on the integrity of red blood cell membranes.²¹ MRI can show absence of enhancement or massive ovarian edema in the case of intermittent torsion, which is shown as diffuse high-signal intensity on T2-weighted images.^15–17 A study by Kato et al. included 14 patients with surgical confirmation of ovarian torsion. Pathologically, hemorrhagic infarction was found in seven of them. They retrospectively reviewed their MRI signal intensity on T1-, T2-, and diffusion-weighted (DW) images in the affected ovary. Signal intensity did not differ significantly on T1-weighted, T2-weighted, and DW images between patients with and without hemorrhagic infarction.¹⁸ On T1-weighted images, some studies reported that torsed ovaries with hemorrhagic infarction showed hyperintensity,^22,23 but others showed hypointensity.²¹ The hyperintensity of enlarged ovarian stroma on T2-weighted images was most likely related to edema secondary to torsion and not hemorrhagic infarction^24,25; however, hypointensity may indicate hemorrhagic infarction.²² Bader et al. reported one case of ovarian torsion with hemorrhagic necrosis where the enlarged stroma appeared hypointense on T2-weighted images.⁵ In Kawakami et al.²² series and in Rha et al.¹⁶ series, no hyperintensity of the stroma on T2-weighted images was reported in hemorrhagic necrosis.

This study sought to determine the value of MRI assessment for diagnosis of ovarian necrosis to decide to preserve the viable adnexa or adnexectomy for non-viable structure. Thirteen women, who were operated on within 3 hours after admission, underwent MRI assessment for necrosis. T1-weighted imaging showed significant hypo-intensity in the case with suspected infarction; the same case remained as grade 4 after detorsion and necessitated adnexectomy, which was proved necrotic by histopathology postoperatively. The analysis of our data shows that MRI has succeeded in suspecting necrosis in cases of AT.

This study is consistent with the earlier studies with regard to the criteria for diagnosis of ovarian torsion depending on clinical, ultrasound, and Doppler findings,^12–16 in addition to MRI diagnostic criteria of torsion and possible necrosis.^24,25 The consistent clinical symptom was abdominal pain localized to a lower quadrant, which was the chief symptom in 100% at the time of presentation; however, vomiting, fever, and leukocytosis were more variable presentations.^1,3,4,19,20

This study is, to our knowledge, the first to date in which decision making for the type of surgical procedure (adnexectomy or detorsion) depends on MRI findings that are suggestive of necrosis. The main limitation of this study is the low number of studied patients due to relative rarity of cases and strict inclusion criteria, in addition to the MRI reading radiologist impressions and experiences. The presence of arterial or venous flow may have caused the pursuit of other diagnoses, and ovaries that may have been viable at the time of MRI evaluation could have progressed to irreversible ischemia in the interval between presentation and surgery. More work is needed, as the idea used in this study needs to be reassessed.

Conclusion

The presentation of AT is nonspecific, with no absolute clinical profile. It is imperative that AT be early diagnosed and surgically managed to preserve ovarian function before ovarian necrosis. MRI may aid in the diagnosis of AT necrosis. In this study, the use of MRI in suspicion of necrosis may be promising; however, more studies are required to support this issue.

Footnotes

Acknowledgment

The authors thank Dr. Manal M. Abdou for her invaluable assistance in all surgical procedures and postoperative care for all studied cases.

Disclosure Statement

No competing financial interests exist.

References

Bar-On

, Mashiach

, Stockheim

, et al. Emergency laparoscopy for suspected ovarian torsion: Are we too hasty to operate?. Fertil Steril, 2010; 93:2012.

Huchon

, Fauconnier

. Adnexal torsion: A literature review. Eur J Obstet Gynecol Reprod Biol, 2010; 150:8.

Warner

, Fleischer

, Edell

, et al. Uterine adnexal torsion: Sonographic findings. Radiology, 1985; 154:773.

Huchon

, Panel

, Kayem

, Schmitz

, Nguyen

, Fauconnier

. Does this woman have adnexal torsion?. Hum Reprod, 2012; 27:2359.

Bader

, Ranner

, Haberlik

. Torsion of a normal adnexa in a premenarcheal girl: MRI findings. Eur Radiol, 1996; 6:704.

McGovern

, Noah

, Koenigsberg

, Little

. Adnexal torsion and pulmonary embolism: Case report and review of the literature. Obstet Gynecol Surv, 1999; 54:601.

Mage

, Canis

, Manhes

, Pouly

, Bruhat

. Laparoscopic management of adenexal torsion, a review of 35 cases. J Reprod Med, 1989; 34:520.

Karayalçın

, Ozcan

, Ozyer

, et al. Conservative laparoscopic management of adnexal torsion. J Turk Ger Gynecol Assoc, 2011; 12:4.

Sasaki

, Miller

. Adnexal torsion: Review of the literature. J Minim Invasive Gynecol, 2014; 21:196.

10.

Oelsner

, Bider

, Goldenberg

, Admon

, Mashiach

. Long term follow-up of the twisted ischemic adnexa managed by detorsion. Fertil Steril, 1993; 60:976.

11.

Oelsner

, Cohen

, Soriano

, Admon

, Mashiach

, Carp

. Minimal surgery for the twisted ischaemic adnexa can preserve ovarian function. Hum Reprod, 2003; 18:2599.

12.

Pena

, Ufberg

, Cooney

, Denis

. Usefulness of Doppler sonography in the diagnosis of ovarian torsion. Fertil Steril, 2000; 73:1047.

13.

Oelsner

, Shashar

. Adnexal torsion. Clin Obstet Gynecol, 2006; 49:459.

14.

Spencer

, Forstner

, Cunha

, Kinkel

. ESUR guidelines for MR imaging of the sonographically indeterminate adnexal mass: An algorithmic approach. Eur Radiol, 2010; 20:25.

15.

Chang

, Bhatt

, Dogra

. Pearls and pitfalls in diagnosis of ovarian torsion. Radiographics, 2008; 28:1355.

16.

Rha

, Byun

, Jung

, et al. CT and MR imaging features of adnexal torsion. Radiographics, 2002; 22:283.

17.

Roche

, Chavan

, Aquilina

, Rockall

. Radiological appearances of gynaecological emergencies. Insights Imaging, 2012; 3:265.

18.

Kato

, Kanematsu

, Uchiyama

, Yano

, Furui

, Morishige

. Diffusion weighted imaging of ovarian torsion: Usefulness of apparent diffusion coefficient (ADC) values for the detection of hemorrhagic infarction. Magn Reson Med Sci, 2014; 13:39.

19.

Tandulwadkar

, Shah

, Agarwal

. Detorsion and conservative therapy for twisted adnexa: Our experience. J Gynecol Endosc Surg, 2009; 1:21.

20.

Wang

, Xie

, Wu

, Li

, Ma

, Wang

. Laparoscopic management of pedicle torsion of adnexal cysts. Oncol Lett, 2013; 5:1707.

21.

Bradley

Jr . MR appearance of hemorrhage in the brain. Radiology, 1993; 189:15.

22.

Kawakami

, Murata

, Kawaguchi

, et al. Hemorrhagic infarction of the diseased ovary: A common MR finding in two cases. Magn Reson Imaging, 1993; 11:595.

23.

Tamai

, Koyama

, Saga

, et al. MR features of physiologic and benign conditions of the ovary. Eur Radiol, 2006; 16:2700.

24.

Ghossain

, Hachem

, Buy

, et al. Adnexal torsion: Magnetic resonance findings in the viable adnexa with emphasis on stromal ovarian appearance. J Magn Reson Imaging, 2004; 20:451.

25.

Greer

, Koroshetz

, Cullen

, Gonzalez

, Lev

. Magnetic resonance imaging improves detection of intracerebral hemorrhage over computed tomography after intra-arterial thrombolysis. Stroke, 2004; 35:491.