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ORIGINAL RESEARCH

Spectrums and Outcomes of Adnexal


Torsion at Different Ages
Jie-Ling Feng, MD, Ting Lei, MD, Hong-Ning Xie, PhD, Li-Juan Li, MD, Liu Du, MD

Objectives—To investigate the role of ultrasound in the preoperative diagnosis of


adnexal torsion and describe its histological spectrum and outcomes at different
ages.
Methods—This study comprised a retrospective investigation of a data set that
included 195 female patients with clinically suspected adnexal torsion between Janu-
ary 2010 and July 2015. Each patient received a detailed pelvic ultrasound examina-
tion by an experienced ultrasound examiner, and a definitive diagnosis was achieved
via surgery. The accuracy of an ultrasonic diagnosis of adnexal torsion was assessed.
The patients were divided into three groups: female children and adolescents, fertile
women, and postmenopausal women. The size, type, histological spectrum, and out-
come of adnexal torsion in the different groups were also described.
Results—The sensitivity, specificity, and accuracy of ultrasound were 0.84, 0.77, and
0.81, respectively. There were significant differences in the presence of ultrasonic
hallmarks among the true positive, false positive, and false negative cases of adnexal
torsion. Ovarian torsion was identified in 94 cases, and isolated tubal torsion was
identified in 15 cases. The most common histologic diagnoses of the pediatric group
and the other two groups were a normal ovary and teratoma, respectively. The most
common histologic diagnoses in the cases of isolated tubal torsion were mesosalpinx
cyst and oviduct inflammation.
Conclusions—Ultrasonography plays an important role in the preoperative diagno-
sis of adnexal torsion. Despite ovarian involvement in most of the cases, isolated ovi-
duct torsion was not uncommon. The spectrum of histological diagnoses varied
among the age groups.
Key Words—adnexal torsion; surgical treatment; ultrasonography

Received November 14, 2016, from the Depart-

A
ment of Ultrasonic Medicine, Fetal Medical dnexal torsion is defined as the twisting by at least one com-
Center, First Affiliated Hospital of Sun Yat-sen plete turn of the ovary, or more rarely the tube alone, around
University, Guangzhou, Guangdong, China.
Manuscript accepted for publication November
a centerline that consists of the infundibulopelvic ligament
28, 2016. and tubo-ovarian ligament.1 Thus, adnexal torsion includes either
This study was supported by research ovarian torsion with or without fallopian tube, or isolated tubal tor-
grant 81571687 from the National Scientific sion. The estimated incidence of adnexal torsion is approximately 2.7
Foundation Committee of China and grant to 3.0%.2
2014BAI06B05 from the National Science- Adnexal torsion is regarded as a gynecologic emergency.3
technology Support Plan Projects. J.-L.F. and
T.L. contributed equally to this work. Female reproductive function is often affected if treatment is delayed
Address correspondence to Hong-Ning as a result of uncertainty in the diagnosis. The clinical symptoms of
Xie, PhD, Department of Ultrasonic Medicine, adnexal torsion are nonspecific and include the sudden onset of
Fetal Medical Center, First Affiliated Hospital severe pelvic pain, nausea, vomiting, and a palpable adnexal mass.4
of Sun Yat-sen University, #58 ZhongShan Er Pelvic ultrasonic examination is commonly performed before surgery;
Road, Guangzhou 510080, Guangdong, China.
E-mail: hongning_x@126.com
however, the findings are nonspecific. The diagnosis of adnexal tor-
sion may only be confirmed by surgery. The accuracy of ultrasound
doi:10.1002/jum.14225 in the diagnosis of adnexal torsion confirmed at surgery varies

C 2017 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2017; 36:1859–1866 | 0278-4297 | www.aium.org
V
Feng et al—Spectrums and Outcomes of Adnexal Torsion

between 23 and 75% in different studies.2,5–8 The preop- to 9-MHz transvaginal probe or an abdominal 4- to 8-
erative diagnosis of adnexal torsion remains a challenge. MHz probe (GE Healthcare, Kretztechnik, Zipf, Aus-
Adnexal torsion can occur at all ages, but the peak tria). A transabdominal/transrectal approach was per-
prevalence is in women of reproductive age.3 The most formed in virgin patients with consent by the individual
common overall histologic diagnosis varied in different or her guardian, and a transvaginal approach was per-
studies.4,9–13 Furthermore, the spectrum of histologic formed in patients who were sexually active.
diagnosis of adnexal torsion at different ages has not The ultrasonic hallmarks of adnexal torsion include
been thoroughly investigated. The histologic diagnosis a unilateral ovarian enlargement (>4 cm) with or with-
of adnexal torsion at different ages may be helpful to out an ovarian mass (Figure 1) or adnexal mass; ovarian
improve the accuracy of diagnosis before operation. edema with the presence of a hyperechogenic ovary and
The aim of this study was to investigate the role of peripherally displaced follicles with echogenic stroma
ultrasound in the preoperative diagnosis of adnexal tor- (Figure 1); abnormal adnexal position; free fluid in the
sion, and describe its histological spectrum and out- Douglas pouch; the absence of or decreased blood flow
comes in different age groups. in the ovary, as demonstrated using Doppler ultrasound
(Figure 1); and the presence of coiled, twisted, or circu-
Materials and Methods lar (ie, “whirlpool”) vessels (Figure 2).15–17 Two of
these ultrasound criteria were required for a diagnosis of
This study consisted of a retrospective investigation of adnexal torsion.
data obtained for 195 female patients with clinically sus- The sensitivity, specificity, positive predictive value,
pected adnexal torsion at the First Affiliated Hospital of negative predictive value, and accuracy of the ultrasound
Sun Yat-sen University, which is a multidisciplinary terti- were evaluated to determine its ability to diagnose ad-
ary center that includes gynecology & obstetrics and nexal torsion. The ultrasonic characters in true positive,
pediatrics, between January 2010 and July 2015. Each false positive, and false negative cases of adnexal torsion
patient received a detailed pelvic ultrasound examina- were compared using chi-square or Fisher’s exact tests.
tion, including the uterus and adnexa, by an experienced The mean and standard deviation were calculated for all
sonographer, and a definitive diagnosis was achieved via measured data. The size of the torsed appendages were
surgery. Each sonographer specialized in obstetrics and compared among the different groups using analysis of
gynecology and had at least 5 years of experience in per- variance and the least-significant difference t-test. P val-
forming obstetric and gynecological ultrasonic diagnoses. ues were considered statistically significant at P < .05.
The study was approved by the institutional review
board of the First Affiliated Hospital of Sun Yat-sen Figure 1. Transabdominal sonogram indicating a unilateral ovary in
University. adnexal torsion. A, Enlarged ovary with ovarian edema. The ovary is
The value of sonography in the diagnosis of adnexal hyperechogenic. The ovarian blood flow decreases. B, Normal-
appearing contra lateral ovary.
torsion was investigated via diagnostic testing. A cohort
of 109 surgically confirmed cases of adnexal cases was
divided into three groups by age. Group 1 included
female children and adolescents who were 18 years old
and younger14; Group 2 included fertile women who
were older than 18 years old and were not postmeno-
pausal; and Group 3 included postmenopausal women.
The types of adnexal torsion included ovarian torsion
with and without the fallopian tube (referred to as ovar-
ian torsion) and isolated tubal torsion. The size, type,
histological diagnosis, and outcome of adnexal torsion in
the different groups were described.
Sonography was performed using a transabdominal,
transvaginal, transrectal, or combined approach as appro-
priate using a GE Voluson730 Expert system with a 5-

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Feng et al—Spectrums and Outcomes of Adnexal Torsion

Statistical analyses were performed using the statistical (2 of 20), ovarian cyst rupture (2 of 20), corpus luteum
software SPSS 13.0 for Windows (IBM Corp, Armonk, hemorrhage (2 of 20), and appendicitis (1 of 20). The
NY). diagnoses of the true negative cases included ectopic
pregnancy (46 of 66), ovarian cyst rupture (13 of 66),
Results ovarian tumor (6 of 66), and tubal mesosalpinx cyst (1
of 66).
Of the 195 clinically suspected cases, 109 cases were A unilateral ovarian enlargement/adnexal mass was
confirmed to be adnexal torsion during surgery. Of the identified in all true positive (91), false positive (20),
111 cases diagnosed as adnexal torsion by ultrasonogra- and false negative (18) cases of adnexal torsion. There
phy, 91 cases agreed with the surgical findings, whereas were 50 true positive cases with ovarian edema; none of
of the 84 cases not indicated to be adnexal torsion by the false positive and false negative cases had ovarian
ultrasonography, 66 cases agreed with the surgical find- edema. Abnormal adnexal positions in the true positive,
ings. Thus, the sensitivity of the ultrasound was 0.84, the false positive, and false negative cases were identified in
specificity was 0.77, the positive predictive value was 7, 8, and 2 cases, respectively. Free fluid in the pouch of
0.82, the negative predictive value was 0.79, and the Douglas in the true positive, false positive, and false neg-
overall accuracy was 0.81. The diagnoses of the false ative cases was present in 26, 9, and 1 case(s), respec-
positive cases included ovarian tumor (9 of 20), pelvic tively. The absence of or decreased blood flow in the
inflammatory disease (4 of 20), heterotopic pregnancy ovary in the true positive, false positive, and false nega-
tive cases occurred in 67, 10, and 9 cases, respectively.
Figure 2. Transvaginal sonogram with a whirlpool sign, indicating the The presence of coiled, twisted or circular (ie, whirl-
presence of coiled, twisted, or circular vessels with Doppler. pool) vessels in the true positive, false positive, and false
negative cases occurred in 63, 8, and 1 case(s), respec-
tively. There were significant differences in the presence
of ultrasonic hallmarks with the exception of the unilat-
eral ovarian enlargement/adnexal mass among the true
positive, false positive, and false negative cases of adnexal
torsion (Table 1).
The 109 true cases of adnexal torsion were divided
into three groups. There were 19 (17.4%) cases in
Group 1 (female children and adolescents); 78 (71.6%)
cases in Group 2 (fertile women), including 19 cases
who were pregnant and 2 cases who induced abortion
within 1 week; and 12 (11.0%) cases in Group 3 (post-
menopausal women). The mean patient age, mean mass
size, torsion side, and torsion types of each group
are listed in Table 2. The mean age of all patients was

Table 1. Ultrasound Findings in True Positive, False Positive, and False Negative Cases of Adnexal Torsion

True Positive False Positive False Negative


Ultrasound Findings Cases (91) Cases (20) Cases (18) P
Unilateral ovarian enlargement/adnexal mass 91 20 18 —a
Ovarian edema 50 0 0 <.001b
Abnormal adnexal position 7 8 2 .01b
Free fluid in the pouch of Douglas 26 9 1 .02c
Absence/decreased of blood flow in the ovary 67 10 9 .04c
Whirlpool sign 63 8 1 <.001b
a
Unilateral ovarian enlargement/adnexal mass occurred in all cases; therefore, no statistics were computed.
b
Comparisons were done using Fisher’s exact tests.
c
Comparisons were done using chi-square test.

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Feng et al—Spectrums and Outcomes of Adnexal Torsion

29.8 6 14.9 years old. The average sizes of the twisted 48 (44%) cases that twisted on the left, whereas 61
mass among all patients and Groups 1, 2, and 3 were (56%) cases twisted on the right.
96.4 6 35.3 mm, 77.2 6 33.0 mm, 95.5 6 34.0 mm, The two types of adnexal torsion included ovarian
and 119.3 6 37.3 mm, respectively. The difference in torsion and isolated tubal torsion. Ovarian torsion was
the mean mass size was significant between Groups 1 identified in 94 (86%) patients. All of these cases had
and 3 as well as Groups 2 and 3, whereas the difference combined ovarian and tubal torsion (Figure 3). Isolated
between Groups 1 and 2 was not significant. There were tubal torsion occurred in 15 (14%) patients. In Group 1,

Table 2. Patient Mean Age, Mean Mass Size, Torsion Side, and Torsion Types at Different Ages

Torsion Side Torsion Types


Group (N) Patient Age (Years) Mass Size (mm) Left Right Ovarian Torsion Tubal Torsion
Group 1 (19) 12.2 6 4.2 77.2 6 33.0 9 10 15 4
Group 2 (78) 29.4 6 8.8 95.5 6 34.0 34 44 67 11
Group 3 (12) 60.0 6 8.4 119.3 6 37.3 5 7 12 0
Total 29.8 6 14.9 96.4 6 35.3 48 61 94 15

Group 1, female children and adolescents; Group 2, fertile women; Group 3, postmenopausal women; ovarian torsion, ovarian torsion
with or without fallopian tube; tubal torsion, isolated tubal torsion.

Figure 3. Ovarian torsion occurring in a 9-year-old girl with severe pelvic pain for 19 hours. A, Transrectal sonogram with color Doppler indicating
an enlarged ovary with ovarian edema and decreased ovarian blood flow. B, Intra-operative findings confirming that the ovary was enlarged and
edematous. C, Transrectal sonogram with color Doppler indicating a torsed pedicle (whirlpool sign). D, Intra-operative findings confirming that
the ovary and tube twisted 7208.

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Feng et al—Spectrums and Outcomes of Adnexal Torsion

ovarian torsion was identified in 15 patients, whereas iso- The most common histologic diagnoses in cases of iso-
lated tubal torsion was identified in 4 patients. In Group lated tubal torsion were mesosalpinx cyst (Figure 5) and
2, ovarian torsion was identified in 67 patients, whereas fallopian tubal inflammation. The histological diagnoses
isolated tubal torsion was identified in 11 patients. All according to age groups are summarized in Table 4.
cases in Group 3 had ovarian torsion. There were no sig-
nificant differences in the torsion patterns among the
three groups. Discussion
The patients were subjected to laparotomy or lapa-
Adnexal torsion is a gynecologic emergency that involves
roscopy: Of the 65 cases treated via adnexectomy, which
the suspensory ligament of the ovary within the broad
removed the affected ovary and fallopian tube, 53 cases
were performed by laparotomy and 12 cases were per- ligament, which contains the lymphatic vessels, veins,
formed by laparoscopy; of the 9 cases treated via salpin- arteries, and nerves that supply the adnexa.17 The differ-
gectomy, 3 cases were performed by laparotomy and 6 ential diagnosis of adnexal torsion includes corpus
cases were performed by laparoscopy; of the 33 cases luteum hemorrhage/rupture, pelvic inflammatory dis-
treated via adnexa detorsion and tumorectomy, 19 cases ease, appendicitis, and ectopic pregnancy.5 A pre-
were performed by laparotomy and 14 cases were per- operative diagnosis is critical, because the complications
formed by laparoscopy; moreover, 2 cases were treated of a delayed diagnosis include the loss of the adnexa or
by adnexa detorsion via laparotomy. Thirty-five patients ovary, fatal thrombophlebitis, or peritonitis.18 Early and
were treated via conservative surgery that involved precise ultrasonic diagnosis of adnexal torsion comprises
adnexa detorsion with or without tumorectomy, and the the basis of treatment. However, the concordance
salvage rate of the ovary was 32% (35 of 109). Sixty-five between ultrasound and surgical diagnoses of adnexal
patients lost adnexa, and 9 patients lost the fallopian torsion varies widely and is predominately affected by
tube. None of the patients experienced other postopera- the ultrasound operator.2,5–8 In our study, we deter-
tive complications. The surgical procedures according to mined the presence of ultrasonic hallmarks varied, with
age group are listed in Table 3. The average hospi- the exception of a unilateral ovarian enlargement/
talization times of all patients and Groups 1, 2, and 3 adnexal mass, among the true positive, false positive, and
were 6.8 6 3.6, 5.8 6 1.9, 6.7 6 3.3, and 9.0 6 6.3 false negative cases of adnexal torsion. This finding sup-
days, respectively. ported that ultrasound examination plays an important
The histological diagnoses were as follows in des- role in the preoperative diagnosis of adnexal torsion.
cending order: teratoma (35 of 109) (Figure 4), normal Ovarian edema was present in 50 true positive cases;
ovary (25 of 109), ovarian cyst (17 of 109), cystade- however, it was not present in the false positive or false
noma (11 of 109), mesosalpinx cyst (9 of 109), oviduct negative cases, which indicated that ovarian edema was a
inflammation (6 of 109), sex cord stromal tumor (4 of reliable ultrasonic marker for adnexal torsion. We
109), and cystadenocarcinoma (2 of 109). The most obtained a high rate of agreement between ultrasound
common histological diagnoses of Groups 1, 2, and 3 examination and surgery for the diagnosis of adnexal tor-
were normal ovary, teratoma, and teratoma, respectively. sion as a result of the use of a specialized obstetrics and

Table 3. Treatment of Adnexal Torsion at Different Ages

Operation Group 1 Group 2 Group 3 Subtotal


Laparotomy Adnexectomy 9 35 9 53
Salpingectomy 0 3 0 3
Adnexa detorsion and tumorectomy 5 14 0 19
Adnexa detorsion 0 2 0 2
Laparoscopy Adnexectomy 1 8 3 12
Salpingectomy 2 4 0 6
Adnexa detorsion and tumorectomy 2 12 0 14
Total 19 78 12 109

Group 1, female children and adolescents; Group 2, fertile women; Group 3, postmenopausal women.

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Feng et al—Spectrums and Outcomes of Adnexal Torsion

gynecology ultrasound unit and a combination of sono- than the left ligament or because of the presence of the
graphic signs to indicate adnexal torsion.16,17 sigmoid on the left, which reduces the space needed for
Adnexal torsion may occur at all ages. It has been torsion to occur.19–21
most frequently reported in women of reproductive age; The twist may involve the ovarian ligament and sus-
however, 15% of cases occur during childhood, and 15% pensory ligament, or it may twist around the Fallopian
of cases occur during or after menopause.3 Our study tube.22 We identified two types in adnexal torsion, which
confirmed these findings that torsion occurred primarily presented as ovarian torsion (with or without the fallo-
in women of reproductive age (71.6%), with 17.4% of pian tube) or isolated fallopian tubal torsion without dis-
cases in children and adolescents and 11.0% of cases in tortion of the ovary. In our study, 94 cases involved
postmenopausal women. There were 19 cases of preg- ovarian torsion, and 15 cases consisted of isolated tubal
nant women, and 2 cases occurred within 1 week of an torsion. The tube often twists with the ovary22; thus, iso-
induced abortion in our cohort, which supports the idea lated fallopian tube torsion is rare and has been reported
that pregnancy is a risk factor for adnexal torsion.11,19 to occur at a rate of 1 in 1.5 million in previous studies.23
The mean size of the torsion mass in the postmeno- In our data, isolated oviduct torsion was not uncommon
pausal women was increased compared with the other and represented approximately 13.8% (15 of 109) of the
groups. Our data also indicated that the right side was total torsion cases, despite the majority of ovarian tor-
dominant in cases of adnexal torsion, likely because the sion. Ovarian torsion was approximately three times as
right utero-ovarian ligament is physiologically longer common as isolated oviduct torsion in female children

Figure 4. Ovarian torsion occurring in a 6-year-old girl who presented with severe pelvic pain for 3 days. A, Transabdominal sonogram indicating
an enlarged ovary with teratoma, and the ipsilateral residual ovary is edematous. B, Transabdominal sonogram with color Doppler indicating a
torsed pedicle (whirlpool sign). C, Intra-operative findings confirming that the ovary was enlarged and edema was present, and the ovary and
tube twisted 7208. D, Patient was treated via adnexa detorsion and tumorectomy.

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Feng et al—Spectrums and Outcomes of Adnexal Torsion

and adolescents; moreover, ovarian torsion was six times common histodiagnosis included a normal ovary, which
as common as isolated oviduct torsion in fertile women. is in contrast to previous studies that reported benign
Interestingly, isolated oviduct torsion was not identified cystic teratomas and hemorrhagic or follicular cysts as
in postmenopausal cases. common causes of torsion.24 Teratoma, followed by a
The most common histological diagnosis has varied normal ovary, was the most common diagnosis in fertile
among studies and includes teratoma, cystadenoma, and women. In postmenopausal cases, teratoma was the
ovarian cyst.3,4,10,11 In our cohort, the most common most common histological type, and none of the cases
diagnosis was teratoma, followed by normal ovary, which was associated with a normal ovary or isolated tubal
supports the idea that ovarian torsion is not only associ- related diseases. Malignant adnexal tumor rarely co-
ated with pathological changes but may also occur in the occurred with torsion25; only two patients in our cohort
normal ovary.13 The histological diagnosis varied among exhibited cystadenocarcinoma torsion at a reproductive
the age groups. In children and adolescents, the most age. An isolated tubal mesosalpinx cyst was one of the
most common causes of isolated fallopian tubal torsion,
which was the fifth most common histology in our
Figure 5. Isolated tubal torsion occurring in a 47-year-old woman cohort.
who presented with pelvic pain for 1 day. Transvaginal sonogram indi- An adnexectomy was conducted when the adnexa
cates the ovary, tubal mesosalpinx cyst, and torsed pedicle (arrow-
heads indicate the whirlpool sign) with 3D render mode. Ova: ovary;
appeared necrotic or did not appear viable after untwist-
Cyst: mesosalpinx cyst. ing the ischemic adnexa, as a general rule.1 Recently,
conservative surgery has been advocated, which typically
involves detorsion of the twisted ischemic adnexa and
ovarian tumorectomy to protect ovarian function.1,9,21
In our cohort, 35 patients were subjected to conservative
surgery, 9 patients underwent a salpingectomy, and the
remaining 65 cases, including all postmenopausal cases,
underwent an adnexectomy because the adnexa were
considered nonviable. Sixty-five patients lost adnexa, and
9 patients lost a fallopian tube. However, none of the
patients experienced other postoperative complications.
These findings suggest that an early preoperational ultra-
sound diagnosis and timely operation are necessary to
improve outcomes.
The limitations of our study include its retrospective
nature and the exclusion of patients not undergoing

Table 4. Histologic Diagnosis at Different Ages

Histologic Diagnosis (N) Group 1 Group 2 Group 3


Ovary (94) Teratoma (35) 5 24 6
Ovary (25) 6 19 0
Ovarian cyst (17) Simple cyst (11) 3 7 1
Hematoma (6) 0 6 0
Cystadenoma (11) Serous cystadenoma (4) 1 2 1
Mucinous cystadenoma (7) 0 6 1
Sex cord stromal tumor (4) Thecoma (2) 0 1 1
Thecofibroma (2) 0 0 2
Malignant tumor (2) Serous cystadenocarcinoma (2) 0 2 0
Fallopian Tube (15) Mesosalpinx cyst (9) 2 7 0
Fallopian tubal inflammation (6) 2 4 0
Total 19 78 12

Group 1, female children and adolescents; Group 2, fertile women; Group 3, postmenopausal women.

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Feng et al—Spectrums and Outcomes of Adnexal Torsion

surgery, which may result in the exclusion of patients 11. Arab M, Tehranian A, Mohammadi AG, Hashemieh M. Review of
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