Diagnosis of Ovarian Torsion with Color Doppler Sonography: Depiction of Twisted Vascular Pedicle

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1 Diagnosis of Ovarian Torsion with Color Doppler Sonography: Depiction of Twisted Vascular Pedicle Eun Ju Lee, MD, Hyuck Chan Kwon, MD, Hee Jae Joo, MD, Jung Ho Suh, MD, Arthur C. Fleischer, MD The purpose of this study was to assess the diagnostic value of ultrasonography for the detection of twisted vascular pedicle in ovarian torsion and to verify whether the blood flow alterations in the twisted vascular pedicle on color Doppler sonography can predict the viability of adnexal structures. In 28 of 32 patients with surgically proved torsion, the twisted vascular pedicle was detected preoperatively by ultrasonography, which shows a diagnostic accuracy of 87%. Arterial and venous flows were present in the twisted vessels on color Doppler sonography in 16 of 28 patients with a visible twisted vascular pedicle. In 11 patients who underwent adnexectomy, the pathologic findings revealed nonnecrotic ovaries in 10 patients. Untwisting of the twisted vascular pedicle was performed in five patients, and follow-up ultrasonography showed normal follicular development and ovulation. All 12 patients who showed no blood flow within the twisted vascular pedicle had necrotic ovaries. In conclusion, identification of the twisted vascular pedicle through ultrasonography is suggestive of ovarian torsion, and color Doppler sonography could be helpful in predicting the viability of adnexal structures by depicting blood flow within the twisted vascular pedicle. KEY WORDS: Ovary, torsion; Adnexa, torsion; Ovary, tumors; Color Doppler sonography. I n adnexal torsion, the ovary or ipsilateral fallopian tube, or both, twists with the vascular pedicle as the axis, resulting in arterial and venous ABBREVIATIONS CDS, Color Doppler sonography; TVS, Transvaginal sonography; TV-CDS, Transvaginal color Doppler sonography Received May 21, 1997, from the Departments of Radiology (E.J.L., J.H.S.), Obstetrics and Gynecology (H.C.K.), and Pathology (H.J.J.), Ajou University, College of Medicine, Kyunggi-do, South Korea; and the Department of Radiology (A.C.F.), Vanderbilt University Medical Center, Nashville, TN. Revised manuscript accepted for publication October 14, Address correspondence and reprint requests to Eun Ju Lee, MD, Department of Diagnostic Radiology, Ajou University Medical Center, San 5, Wonchon-dong, Paldal-gu, Suwon, Kyunggi-do, , South Korea. compromise. Unrelieved torsion is likely to be followed by hemorrhagic infarction as the degree of arterial occlusion progresses. Therefore, early diagnosis of torsion can prevent irreversible damage to the adnexal structures and may contribute to conservative treatment, which may spare the ovary in young women. Ovarian torsion is frequently associated with an ipsilateral ovarian mass (50 to 81%), which may act as fulcrum to potentiate torsion of adnexa due to increased ovarian volume or intraabdominal pressure. 1,2 Adnexal torsion is often difficult to distinguish from other acute abdominal conditions; however, the possibility of ovarian torsion should be considered when an ovarian mass is discovered in the appropriate clinical setting. The variable sonographic findings of the twisted ovary including a solid, cystic, and complex mass with free fluid, diffusely enlarged ovary containing one or more large cystic follicles at the periphery, and marked thickening of the cyst 1998 by the American Institute of Ultrasound in Medicine J Ultrasound Med 17:83 89, /98/$3.50

2 84 OVARIAN TORSION: TWISTED VASCULAR PEDICLE J Ultrasound Med 17:83 89, 1998 wall, have been described. 3 5 However, these features are nonspecific and focus on the twisted ovary itself, which is not detectable in many cases, especially if associated with an ovarian tumor. Therefore, these findings cannot be used as diagnostic criteria in all cases of ovarian torsion. The role of CDS in the early diagnosis of ovarian torsion with depiction of an enlarged ovary that has no demonstrable perfusion in the parenchyma has been reported previously in some cases, but it is still not fully established. 6 8 The purposes of this study were to describe a sonographic finding that may suggest the preoperative diagnosis of ovarian torsion, to assess the diagnostic value of ultrasonography for the depiction of the twisted vascular pedicle in ovarian torsion, and to verify whether the blood flow alteration in the twisted vascular pedicle on CDS can predict the viability of the adnexal structures. MATERIALS AND METHODS For a period of 2 years, 47 patients who were admitted for acute or intermittent lower abdominal pain with a palpable pelvic mass or previous history of ovarian tumor were investigated with both ultrasonography and CDS for ovarian torsion. Sonography was performed transvaginally and transabdominally with Ultramark 9-HDI system (Advanced Technology Laboratories, Bothell, WA) using a MHz curved array or 5.0 MHz curved array transvaginal probe in all patients with the exception of four patients who were virginal or pregnant; these four were examined only transabdominally. To optimize the CDS images, the following parameters were applied: spatial peak temporal average intensity set at approximately 40 to 92 mw/cm 2 and the wallfilter at 50 to 100 Hz, pulse repetition frequencies between 2 and 10 khz, and velocity range lowered to 4 to 20 cm/sec. The Doppler angle of insonation was less than 60 degrees. A minimum of three waveforms were recorded from the twisted vessels within the twisted vascular pedicle. The patients ranged in age from 20 to 70 years (mean, 32.1 years). The clinical findings, including symptoms, history of associated pregnancy, and laboratory findings, were obtained from the patients medical records. We evaluated the presence of twisted vascular pedicle in twisted ovaries by ultrasonography. Normally the vascular pedicle of the ovary, which connects the ovary with uterus and envelops the adnexa and ovarian branches of the uterine artery and vein, appears to have a course that may be either straight or tortuous of intrapedicular blood vessels on ultrasonography and CDS. We defined the twisted vascular pedicle as the rotation site of the vascular pedicle of ovary. It was identified either adjacent to the ovary or ovarian tumors or as a structure visualized separately between the uterus and ovary on the side of the twisted adnexa. Torsion was excluded if we could not detect the twisted vascular pedicle or if the blood vessels within the vascular pedicle had a straight course. In cases in which we could detect the twisted vascular pedicle, torsion was diagnosed on the basis of this finding, and the diagnostic accuracy of twisted vascular pedicle was evaluated. The different morphologic characteristics of the twisted vascular pedicle, including size, shape, internal echogenicity, and visibility of internal vascular structures, were evaluated. The twisted vascular pedicle was measured at its greatest diameter. Color flow sonography and pulsed Doppler sonography were performed to depict the presence or absence of arterial and venous flow within the twisted vascular pedicle and to verify alteration of flow patterns. We considered the adnexal structure potentially viable if blood flow within the twisted vascular pedicle was present, and correlation with the pathologic findings of the affected ovaries, tubes, and tumors was performed. Ovarian torsion was confirmed at the time of surgery in 32 patients. The degree of torsion was determined and gross inspection of the affected adnexal structures was carried out. Salpingooophorectomy and oophorectomy were performed in 22 patients and five patients, respectively. Untwisting of the twisted adnexa with cystectomy or fluid aspiration was performed in the remaining five patients. For those 15 patients whose ovaries were not twisted, pathologic diagnosis of ovarian masses revealed hemorrhagic cyst (follicular, corpus luteal, lutein cyst) in 12 cases, endometrioid cyst in two cases, and tuboovarian cyst in one case. RESULTS Of 32 patients with surgically confirmed ovarian torsion, 25 patients had lower abdominal pain. Acute pelvic pain was present for a period of from 6 hours to 2 days in 21 patients, and chronic intermittent pain was present in four patients for up to 10 months prior to admission. A palpable pelvic mass in 20 patients, tenderness on pelvic examination in 13 patients, and leukocytosis in seven patients were noted. Thirteen patients had a past history of the ovarian tumor and five patients were pregnant (9 to

3 J Ultrasound Med 17:83 89, 1998 LEE ET AL weeks gestation). Surgery was performed within 48 hours after sonographic study in all patients. The side of torsion was on the right in 15 patients and on the left in 17 patients, and the degree of torsion was ranged from 180 degrees ( 1 / 2 complete twist) to 2160 degrees (six complete twists). Pathologic diagnosis of ovarian masses included teratoma in 15 cases, serous and mucinous tumor in five cases (three cystadenoma, two borderline malignancy), endometrioid carcinoma in one case, fibroma in one case, follicular cyst in four cases, and corpus luteum cyst in five cases. At sonography, an ovarian mass was detected on the side of torsion in all patients. The diameters of the ovarian masses ranged from 5 to 33 cm; 17 cases were mostly cystic masses and 15 cases were cystic and solid masses. Twenty-two cases had free fluid in the cul-de-sac. Only four cases had demonstrable ovarian parenchyma on the affected side. In 28 of 32 patients with surgically proved torsion the twisted vascular pedicle was detected preoperatively by ultrasonography, showing a diagnostic accuracy of 87%. Two false-positive cases occurred in which the ovaries were not twisted and in which the preoperative ultrasonograms showed the twisted vascular pedicle. One case was a follicular cyst with subacute salpingitis, and the other was a hemorrhagic corpus luteum cyst with edematous salpinx. The sensitivity and specificity of ultrasonography for the detection of twisted vascular pedicle in ovarian torsion were 88% and 87%, respectively. The positive and negative predictive values were 93% and 76%, respectively. In the other four patients with ovarian torsion, the twisted vascular pedicle was not visible on sonography. All four cases had 360 degrees of torsion or less (one case with 180 degrees, three cases with 360 degrees). Only transabdominal sonography was performed in one virginal patient and one pregnant patient. Of these false-negative cases, three were malignant ovarian tumors, including two cases of serous and mucinous tumor of borderline malignancy and one case of endometrioid carcinoma. The shape and echogenicity of the sonographically visible twisted vascular pedicle varied depending on different views of the structure. The twisted vascular pedicle appeared as a round echogenic mass with multiple concentric hypoechoic stripes (target appearance) in 11 cases, as a beaked appearance with concentric hypoechoic stripes in five cases, or as an ellipsoid or tubular mass with internal heterogeneous echoes in 12 cases. We were able to distinguish the vascular structures within the twisted vascular pedicle on gray scale image in 13 patients but not in the other 15 patients. If the blood flow was present in the twisted vessels within the twisted vascular pedicle on CDS, the characteristic finding of circular or coiled twisted vessels, the so-called whirlpool sign, was presented in 16 cases (Fig. 1). Thirteen patients with blood flow seen on CDS and the vascular structure identified on gray scale sonography had either the target (n = 11) or the beaked (n = 2) appearance, whereas three patients with visible flow on CDS but no vascular structure seen on gray scale sonography had either a beaked appearance (n = 2) or an ellipsoid mass with heterogeneous echoes (n = 1). Thus, documentation of these typical circular vessels on CDS helped to identify the twisted vascular pedicle and to make the diagnosis of torsion. The size of the twisted vascular pedicle ranged in diameter from 2 to 8 cm (mean, 4.2 cm). In 15 cases of torsion of 360 degrees (one complete twist) or less, the twisted vascular pedicles were smaller in diameter, ranging between 2 and 4 cm, and had a target or beaked appearance with identifiable vascular structures within the pedicle. On the other hand, in 13 cases of torsion of more than 360 degrees, the twisted vascular pedicles were large in diameter, ranging between 3.5 and 8 cm, and had a tubular or ellipsoid appearance with heterogeneous echoes, and the vascular structures not identified within the pedicle. In 16 of 28 patients with a visible twisted vascular pedicle, arterial and venous flows were present within the twisted vascular pedicle on CDS. Eleven patients underwent adnexectomy, and their pathologic findings showed normal ovary in six cases, edema and early hemorrhage in each of two cases, and hemorrhagic infarction in one case. One patient with pathologically confirmed hemorrhagic infarction had absent end diastolic flow of arterial waveform (Fig. 2). In the remaining five patients whose ovaries were considered potentially viable by preoperative CDS and by visual inspection at surgery, untwisting of the twisted vascular pedicle was performed. Three of five patients, two with teratoma and one with cystadenoma, were treated by cystectomy. In the remaining two patients with corpus luteal cyst, only fluid aspiration was performed to untwist the vascular pedicle. Subsequent follow-up sonography and CDS performed 3 days to 8 weeks after the detorsion procedure revealed the presence of both arterial and venous flow as well as evidence of normal follicular development and ovulation. The remaining 12 patients showed no blood flow within the twisted vascular pedicle on CDS, and all of them demonstrated hemorrhagic infarction of the adnexal structures (Fig. 3).

4 86 OVARIAN TORSION: TWISTED VASCULAR PEDICLE J Ultrasound Med 17:83 89, 1998 DISCUSSION Ovarian torsion is caused by rotation of the ovary or adnexa with the vascular pedicle on its axis, resulting in arterial, venous, or lymphatic obstruction. It is an acute condition that requires prompt surgical intervention to save the ovary. The ultrasonographic findings in ovarian torsion have been described as a cystic, solid, or complex mass with or without pelvic fluid, thickening of the wall, and cystic hemorrhage. However, these findings are not specific for ovarian torsion, and it is difficult to distinguish them from the findings seen in the other disease, such as hemorrhagic cyst, endometriosis, pelvic inflammatory disease, and ectopic pregnancy. 1,2,4 Previous reports suggested that the presence of multiple peripherally located follicles in a case of unilateral enlarged ovary might be the specific finding of ovarian torsion, but this feature was not always observed. 3 5 Moreover, sonographic appearances of ovarian torsion are more closely related to the duration and degree of torsion, complete or incomplete, and the presence or absence of an associated intraovarian mass or hemorrhage. 8,9 The ovarian parenchyma was not identifiable in many cases in our study, thereby making it more difficult to document the intraovarian flow as well as making this ovarian finding less useful in the diagnosis of torsion associated with an ovarian tumor. Although previous studies have focused exclusively on the ovary or the associated ovarian mass, we placed more emphasis on the observation of the twisted vascular pedicle of affected ovary, which corresponds to the broad ligament, fallopian tube, and adnexal and ovarian branches of the uterine artery Figure 1 27 year old patient with 360 degree torsion of the left ovary and teratoma at 9 weeks of gestation. A, TVS shows a 2 cm round mass with a target appearance (arrows) adjacent to the ovarian tumor, indicating a twisted vascular pedicle. B, TV-CDS shows circular vascular structures within the twisted vascular pedicle ( whirlpool sign). C,D, Color Doppler flow velocimetry demonstrates arterial (C) and venous (D) flow of the vascular structures within the twisted vascular pedicle. Pathologic examination revealed nonnecrotic ovary and tube. A B C D

5 J Ultrasound Med 17:83 89, 1998 LEE ET AL 87 and vein. The twisted vascular pedicle in ovarian torsion was identified by ultrasonography in 88% of the cases of torsion. Therefore, the previously described findings suggested that the presence of the twisted vascular pedicle on ultrasonograms could be a valuable diagnostic sign of the ovarian torsion, with a higher detection rate than the previously described sonographic findings of the twisted ovary or the ovarian masses; the detection rate of a cystic, solid, or complex mass was between 46 and 74%, and that of multiple peripherally located follicles in enlarged ovary was 64%. 2 4 The twisted vascular pedicle appeared as a round hyperechoic structure with multiple concentric hypoechoic stripes (target appearance), as a beaked structure with concentric low echoic stripes, or as an ellipsoid or tubular structure with internal heterogeneous echoes. Concentric low echoic intrapedicular structures could be identified as vascular structures by CDS ( whirlpool sign ), and this finding might be useful in the diagnosis of ovarian torsion. Although the detection of the twisted vascular pedicle was difficult when no blood flow was present in the intrapedicular vessels, in our experience it was not impossible to detect the twisted vascular pedicle in this condition. In cases with a relatively small twisted vascular pedicle and torsion of less than 360 degrees, technical difficulty often resulted in a false-negative diagnosis. It was also difficult to identify the twisted vascular pedicle by the transabdominal approach, which was used only in virginal or pregnant women, and the diagnosis of malignancy preceded the diagnosis of ovarian torsion in patients with malignant Figure 2 35 year old patient with 720 degree torsion of the left ovary and teratoma. A, TVS shows a 4 cm round mass with heterogeneous echoes (arrows) lateral to the ovarian tumor. B,TV-CDS shows vascular structures with a whorled appearance within the twisted vascular pedicle. C, Color Doppler flow velocimetry demonstrates arterial and venous flow within the vascular structures, but end diastolic flow of the artery is absent. D, Excised specimen shows the twisted vascular pedicle and ovary as well as teratoma with hemorrhagic necrosis. A B C D

6 88 OVARIAN TORSION: TWISTED VASCULAR PEDICLE J Ultrasound Med 17:83 89, 1998 ovarian tumor. On the other hand, a false-positive diagnosis could be made in cases of ovarian tumor associated salpingitis, endometriosis, or hemorrhagic cyst associated edema, since these conditions could have similar findings. In fact, two false-positive diagnoses were made in patients with follicular cyst and hemorrhagic corpus luteum cyst associated with salpingitis or edema; in these cases dilated and tortuous vessels within vascular pedicle were misdiagnosed as the twisted vascular pedicle. TVS and CDS are expected to demonstrate the ovarian blood supply, and there have been few reports of an enlarged ovary with absent or markedly diminished ovarian blood flow as a specific finding for the early diagnosis of ovarian torsion using CDS. 6,7 Other studies demonstrated the presence of normal arterial flow in three confirmed cases of ovarian torsion, which suggested the venous thrombosis without arterial occlusion and dual blood supply of the ovary as a possible explanation for the symptoms of ovarian torsion. 8 These different results indicated that in partial torsion or earlier stages of torsion, before arterial occlusion, both arterial and venous flow could be maintained with viable ovarian tissue. The most common method for treatment for ovarian torsion has been adnexectomy without untwisting because of the fear of thromboembolism from a thrombosed vein of the twisted ovary, the possibility of retorsion, and the inability to determine the viability of the ovary. However, several papers have reported the practice of untwisting of the vascular pedicle not only to conserve ovarian function but also to preserve fertility without thromboembolism after detorsion In an attempt to ascertain the viability of the ovarian tissue for conservative management of the twisted adnexa, gross inspection or the application of intravenous fluorescent dye at surgery has been used, but this technique proved to be difficult to perform preoperatively. 13 However, sonography with color Doppler imaging may be used to predict the ovarian tissue viability by demonstrating ovarian blood flow. Recent reports have suggested that documentation of intraovarian venous flow was important in establishing the viability of the affected ovaries. 9 Other experimental data have shown that the arterial waveforms in chronic torsion mimic venous ones. 14 In this study, we performed CDS in the twisted vascular pedicle, instead of the ovarian parenchyma, to assess the viability ovary in cases of torsion. All patients who showed no blood flow within the twisted vascular pedicle on CDS demonstrated hemorrhagic infarction and necrosis of the adnexal structures. Of 16 patients with arterial and venous flow within the twisted vascular pedicle on CDS, 15 patients had nonnecrotic ovaries on pathologic examination or viable ovaries on follow-up sonography after untwisting of the vascular pedicle, showing 94% predictability of the viability of the adnexal structure. Therefore, the presence of arterial and venous intrapedicular flow was correlated with nonnecrotic adnexa on pathologic examination and might aid in differentiating potentially viable ovaries from nonviable ovaries. However, the waveform of arterial flow showed absent end diastolic flow in one patient with pathologically confirmed hemorrhagic Figure 3 56 year old patient with 720 degree torsion of the right ovary and teratoma. A, TVS shows a 6 4 cm round mass with heterogeneous echoes (arrows) adjacent to the ovarian tumor. B, TV-CDS demonstrates no blood flow within the twisted vascular pedicle. Pathologic examination revealed hemorrhagic necrosis of the ovary and tube. A B

7 J Ultrasound Med 17:83 89, 1998 LEE ET AL 89 infarction. Therefore, if arterial and venous flow were maintained in the intrapedicular vessels, decreased or absent arterial end diastolic flow could be interpreted as a sign of nonviability of the adnexal structures. In this study, the patients who had intrapedicular blood flow on CDS were treated conservatively by untwisting of the vascular pedicle to preserve the ovary. In these conservatively managed cases, none showed thromboembolism or retorsion, and subsequent sonography revealed normal ovaries with follicular development and ovulation. These results suggest CDS findings of flow within the twisted vascular pedicle could indicate viability of adnexal structures. Nevertheless, it is still unclear if the sonographic findings, intraoperative visual impression, and pathologic findings are sufficient to decide whether there is a chance of ovarian preservation or not. Therefore, the correlation of CDS diagnosis of presence or absence of blood flow within the twisted vascular pedicle and the possibility of ovarian viability after detorsion should be investigated in a long-term follow-up study. In conclusion, it is suggested that the identification of the twisted vascular pedicle through ultrasonography is suggestive of ovarian torsion and it may be useful in preoperative diagnosis of this pathologic condition. CDS can be helpful in predicting the viability of the twisted adnexal structures by depicting arterial and venous flow within the twisted vascular pedicle, and it may allow prediction of which patients may undergo conservative management of ovarian torsion. REFERENCES 1. Hibbard LD: Adnexal torsion. Am J Obstet Gynecol 152:456, Warner MA, Fleischer AC, Edell SL, et al: Uterine adnexal torsion: Sonographic findings. Radiology 154:773, Graif M, Shalev J, Strauss S, et al: Torsion of the ovary: Sonographic features. AJR 143:1331, Graif M, Itzchak Y: Sonographic evaluation of ovarian torsion in childhood and adolescence. AJR 150:647, Helvie MA, Silver TM: Ovarian torsion: Sonographic evaluation. J Clin Ultrasound 17:327, Van Voorhis BJ, Schwaiger J, Syrop CH, et al: Early diagnosis of ovarian torsion by color Doppler ultrasonography. Fertil Steril 58:215, Desai SK, Allahbadia GN, Dalal AK: Ovarian torsion: Diagnosis by color Doppler ultrasonography. Obstet Gynecol 84:699, Rosado WM Jr, Trambert MA, Gosink BB, et al: Adnexal torsion: Diagnosis by using Doppler sonography. AJR 159:251, Fleischer AC, Stein SM, Cullinan JA, et al: Color Doppler sonography of adnexal torsion. J Ultrasound Med 14:523, Bayer AI, Wiskind AK: Adnexal torsion: Can the adnexa be saved? Am J Obstet Gynecol 171:1506, Wagaman R, Williams R: Conservative therapy for adnexal torsion. J Reprod Med 35:833, Ben-Rafael Z, Bider D, Mashiach S: Laparoscopic unwinding of twisted ischemic hemorrhagic adnexum after in vitro fertilization. Fertil Steril 53:569, McHutchinson LB, Koonings P, Ballard C: Preservation of ovarian tissue in adnexal tissue with fluorescein. Am J Obstet Gynecol 168:1386, Bude RO, Kennelly MJ, Adler RS, et al: Nonpulsatile arterial waveforms: Observation during graded testicular torsion in rats. Acad Radiol 2:879, 1995