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Gynecological Endocrinology, 2012; Early Online: 1-5
© 2012 Informa UK, Ltd.
ISSN 0951-3590 print/ISSN 1473-0766 online
DOI: 10.3109/09513590.2012.705377
Review Article
dnexal torsion in children and adolescents: new trends to conservative
A
surgical approach – Our experience and review of literature
Claudio Spinelli1, Irene Buti1, Valentina Pucci1, Josephine Liserre1, Elisabetta Alberti1, Luca Nencini2,
Martin Alessandra3, Roberto Lo Piccolo3 & Antonio Messineo3
1Department of Surgery, Chair of Pediatric Surgery, 2Faculty of Mathematical, Physical and Natural Sciences, University of Pisa, Italy,
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and 3Department of Pediatric Surgery, Children’s Hospital A. Meyer, University of Florence, Italy
The purpose of this study is to discuss the surgical treatment for
ovarian torsion in children and adolescents with a focus on the
procedures of adnexal conservation surgery and its frequency
in the literature of the last 10 years. We retrospectively reviewed
the medical charts of 127 operative ovarian lesions including 30
ovarian torsions (23.6%) treated in two pediatric centers over
a 10-year period. Age at presentation, presenting symptoms,
diagnostic studies, surgical procedure and pathological findings were analyzed. Mean age was 13.7 years. Conservative
surgery has been performed in 46.7% of the cases and laparoscopic approach in 40%. Ovarian torsion occurred in 56.7% on
ovaries with functional lesion, in 23.3% on normal adnexa and
in 20% on ovaries with benign neoplasm. The article includes
a literature review (2000–2010) and a statistical analysis which
shows a slow increase in conservative surgery from 28 to 45%.
Laparoscopic surgery accounts for 23.5%. Literature review
shows 40.5% normal adnexa, 33.2% non-neoplastic lesions,
25.3% benign neoplasms and 1% malignant neoplasms. The
surgical treatment of children and adolescents presenting
adnexal torsion should be practiced as an emergency and it
should be more conservative as possible in order to maximize
the future reproductive potential.
[5,13]. The resection of the affected adnexa, called as radical
treatment, can have a negative impact on fertility, especially in
case of recurrence or bilaterality [15], while adnexal conservation surgery, performed as soon as possible, seems to be the best
surgical approach in order to maximize the future reproductive
potential of the girl. The danger of missing malignant pathology,
the risk of thromboembolic complication and the fear that a severe
ischemic ovary is non-viable, have led the use of oophorectomy
[1,2,14,16–20]. Several studies show a low risk of malignancy
and thromboembolism associated with ovarian torsion, and that
the macroscopic appearance of ovary is not a true indicator of
the degree of ischemia [1,11,21]. These pieces of evidence have
suggested the possibility of more conservative surgical treatment.
The purpose of this article is to report our experience on the
surgical approach to ovarian torsion in children and adolescents,
presenting 30 cases, a literature review of the last 10 years with
statistical analysis including 3858 cases.
Materials and methods
This study included all pediatric cases with ovarian masses
surgically treated from 2001 to 2010 at our institutions. After the
Institutional Review Board approval, the informed consent was
obtained from all parents prior to the study. Age at operation and
presenting symptoms were analyzed for each patient. Clinical
examination, trans-abdominal Ultrasonography (US) and Color
Doppler Ultrasonography have been performed in all patients,
while selected patients underwent trans-vaginal Ultrasound,
standard abdominal x-ray examinations, Computed Tomography
(CT), Magnetic Resonance Imaging (MRI) and evaluation of
serum tumor markers (CA-125, α-FP, β-hCG and CA-19.9).
The nature of the masses was defined by histopathological
features using intraoperative frozen section with definitive
histological analysis. The histological diagnosis followed the
WHO classification [22]. Surgical procedures were led by
laparoscopic or open surgery and were performed using either
the conservative or the radical approach. Adnexal conservation
treatment was practiced as detorsion alone or detorsion followed
by subsequent surgical cystectomy or tumorectomy with ovarian
tissue preservation and eventually oophoropexy. All children
treated conservatively underwent US follow-up at postoperative
weeks 1, 4 and 8, then every 3 months up to 1 year.
This article includes a literature review carried out using
PubMed and Ovid to research articles published from 2000 to
Keywords: adolescents, children, conservative approach, ovarian
disease, ovarian torsion, ovarian surgery
Introduction
Ovarian torsion is the twisting of the ovary on its vascular
support. When ovarian torsion remains undiagnosed, blood
supply becomes compromised resulting in tissue necrosis. It is
important to make an immediate diagnosis and provide treatment in order to save the ovary. Ovarian torsion can occur at
all ages, pediatric cases represent the 15% [1], and the estimated
incidence is 4.9/100,000 females aged 1–20 years [2]. The twisting
of the ovary may involve a normal ovary or an ovary with functional pathology, benign or malignant neoplasm [3,4]. In children
torsion on a normal ovary is more frequent because of the greater
length of the ovarian pedicle [5–10]. An abnormally long fallopian
tube, mesosalpinx or mesoovarium causes an excess of mobility
of the adnexa, determining a higher risk of torsion [5,6,11–14].
The clinical presentation of ovarian torsion is unspecific and, at
the present time, there is not a reliable method to confirm the
diagnosis pre-operatively, sometimes diagnosis is during surgery
Correspondence: Prof. Claudio Spinelli, M.D., Department of Surgery, Chief of the Chair of Pediatric Surgery, University of Pisa, Via Paradisa 2,
56124 Pisa, Italy. Tel: (+39) 050–997-702. Mob: (+39) 333-40-69-061. Fax: (+39) 050–997-707. E-Mail: [email protected]
1
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2 C. Spinelli et al.
2010, responding to entries such as “ovarian torsion,” “adnexal
torsion,” “pediatric and adolescence” and those deemed to
provide the greatest contributions in the surgical strategy of
ovarian torsion in children were selected in this review. The
search found 24 articles [2,6–9,11–13,15–18,21,23–32] and they
has been analyzed for several ovarian torsion’s features: right-left
side, histopathology results and surgical details – as the laparoscopic or open approach, as the conservative or radical treatment
and the oophoropexy practice. The surgical treatment grouped in
conservative or radical surgery has been reported by all articles
considered, with a total of 3858 cases; the histopathology results
grouped in normal ovaries, non-neoplastic lesions (follicular and
hemorrhagic cysts), benign ovarian neoplasm and malignant
ovarian neoplasm, include 1734 cases [2,6–9,11–13,15–18,21,23–
28,30–33]. The right-left side, the surgical approach (laparoscopy
or laparotomy) and the oophoropexy practice were described for
a total of 298 [2,6–9,11–13,15–18,21,25–28,30,31,33,34] cases.
The surgical strategy has been carefully evaluated and, with the
aim of highlighting differences over time, a statistical analysis of
cases of ovarian torsion treated with conservative surgery over the
last 10 years, was included. For this purpose, the data obtained
from literature searches have been previously filtered by rejecting
any case reports or any other publications specifically aimed to
the exclusive study of only one of the two surgery treatments.
Statistical analysis was done using 1-Tail Spearman correlation to
assess the correlation between conservative surgery and radical
surgery [35].
Results
Over a 10-year period, 127 surgical interventions for ovarian
lesions in 120 children and adolescents have been evaluated (7
presented asynchronous bilateral lesions). Ovarian torsion cases
were 30, in 29 children with a mean age of 13.7 years (from 2
months to 18 years). We observed: 61 (48%) functional cysts; 54
(42.5%) benign neoplasms and 5 (4.0%) malignant neoplasms.
The ovarian torsion occurs on ovary with hemorrhagic cysts in
10 cases (33.3%), follicular cysts in 7 cases (23.3%), mature cystic
teratomas in 5 cases (16.7%) and cystadenoma in one case (3.3%);
there were 7 torsions (23.3%) on normal ovaries, including one
asynchronous recurrence of a left normal ovary 8 month later the
right one (Figure 1). Abdominal pain was the main symptom for
ovarian torsion, presenting acute pain in 26 cases (89.6%) and
cyclic pain in 3 (19.4%); nausea and vomiting occurred in 17 cases
(56.7%) and 6 cases (20%) presented fever. The white blood cell
count was elevated 63.3% of the time with a mean count of 12500
cells/mm3. Median delay between initial onset of symptoms and
surgery was 12 h (range: 7 h–4 days). Torsion occurred on the
right side in 21(70%) patients and on the left in 9 (30%) patients.
Imaging studies of patients with ovarian torsion included transabdominal and color doppler US in all cases, trans-vaginal US in
6 cases (20%), standard abdominal x-ray examinations in 10 cases
(33.3%), CT and MRI in 8 cases (26.7%). The sonographic appearance of the lesions was: simple lesions for all follicular cysts and
2 hemorrhagic cysts (20%); complex lesions for 8 hemorrhagic
cysts (80%), 3 mature cystic teratomas (60%) and one cystadenoma; solid lesion for 2 mature cystic teratomas (40%). Ovarian
enlargement and the presence of small cystic structures around
the periphery of the ovary were the sonographic appearance of
the ovarian torsion on normal ovaries. The mean diameter of the
ovary, measured by ultrasound, was 6.7 cm (from 5.1 to 13 cm).
Free fluid in the Pouch of Douglas was present in 8 cases (26.7%).
Preoperative Color Doppler Ultrasonography examination
revealed decreased or absent blood flow to the involved ovary
in 19 cases (63%) and normal in 11 cases (37%). Because of the
clinical emergency, tumor marker levels have been measured in
16 cases, and they were high in one case: α-FP > 12 ng/ml in presence of a mature cystic teratoma complicated by ovarian torsion.
This value has normalized 1 month after surgery.
We used a laparoscopic approach in 12 patients (40%) and
the open one in 18 (60%). The cases practiced in open were
performed mostly in the first period of observation. Adnexal
conservation surgery was performed in 14 cases (46.7%) and the
surgical procedures were detorsion alone in 5 children (35.7%)
with normal ovaries, including 4 ovaries presenting a blackbluish macroscopic appearance at surgery; detorsion followed by
cystectomy in 8 children (57.1%) with 4 hemorrhagic cysts and
4 follicular cysts; detorsion followed by tumorectomy in one girl
(7.2%) with a mature cystic teratoma.
The resection of the affected adnexa was necessary in 16 children (53.3%) because the ovarian tissue necrosis had progressed.
Radical treatment occurred on 9 functional lesions (56.3%), 2
normal ovaries (12.5%), and 5 neoplastic benign lesions (31.2%).
Oophoropexy was performed in 4 cases (13.3%). All these torsions
occurred on the left ovary, and we practiced oophoropexy by
fixing the right ovary to the lateral part of the pelvic wall in 2
cases, and to the posterior wall of the uterus in the other 2 cases.
US follow-up was performed in all children treated by conservative surgery, and in all cases, including black-bluish ovaries,
we observed recovery of the ovarian tissue with ovarian volume
normalization, nearly like the contralateral, in a time between 3
and 6 months.
Our literature review about ovarian torsion considered a total
of 3858 pediatric cases with mean age of 14 years. The surgical
treatment was radical in 2377 cases (61.6%) and conservative in
1481 cases (38.4%). The ovarian histopathology finding includes
1734 cases. The pediatric torsion occurs on normal ovary in 703
cases (40.5%), on ovary with non-neoplastic lesions in 575 cases
(33.2%) and on ovary affected by benign ovarian neoplasms in
438 cases (25.3%). Ovarian torsion in presence of malignancy
happened in 18 cases (1%).
The right-left side, the laparoscopic or open approach, and
the oophoropexy practice were described for a total of 298 cases
and they were respectively: 184 right ovaries (61.7%), 228 cases
with laparotomy approach (76.5%) and 23 oophoropexy practice
(7.2%).
The graph in Figure 2 shows the statistical analysis which presents, on the horizontal axis, the median year for the period during
which the study was performed and each point, corresponding
to the axis of ordinates, is associated with the percentage of work
performed by conservative surgery. The median years coinciding
with separate studies, are analyzed cumulatively. The size of the
circles is directly proportional to the number of cases. It was
finally calculated a linear weighted average of the number of cases
accumulated for each year median. The graph shows an increasing
trend of cases treated with conservative surgery, from 28% to 45%
related to 1990 and 2010 respectively. The Spearman’s R for the
two surgical approaches, conservative and radical, is 0.122 (p <
0.01 one tail) permitting to consider the analysis to be significant.
Discussion
Ovarian torsion accounts for up to 2.7% of all cases with acute
abdominal pain in children 18,26. This is the main symptom,
presented in 83% to 100% of cases [7,13,31], and it may be associated with other symptoms, such as fever (from 18% to 22%)
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Surgery for ovarian torsion 3
Figure 1. Histopathological analysis of total ovarian masses and the correlation between ovarian lesion and torsion. Black: no torsion; Gray: torsion.
Figure 2. Statistical analysis of literature review for pediatric ovarian torsion
cases treated with conservative surgery from year 2000 to 2010. The size of
circles is directly proportional to the number of cases. Spearman’s R is 0.122
(p < 0.01 one tail).
[31,32,36], nausea and vomit (from 59% to 85%) [26,31,36].
Therefore its clinical presentation is unspecific and it can mimic
many abdominopelvic surgical diseases. Unfortunately only
about one half of the patients are suspected of adnexal torsion
at the time of the first clinical diagnosis, it is often confused
with acute appendicitis also for possible presence of leucocytosis
(50–82%) [8,21,26,32,36]. Although acute presentation is more
frequent, patients ranging from 4% to 28% present a history of
cyclic abdominal pain, this is due to torsion and spontaneous
detorsion of the ovary [8,11,14,15,31]. During the diagnostic
stage, abdominal mass effect and calcification on plain x-ray study
suggest the presence of mature cystic teratoma [13,14,16,24], but
ultrasonography is the primary diagnostic method employed
for the evaluation of suspect ovarian torsion [17,37,38]. The
most common sonographic finding of torsion in normal ovaries
is ovarian enlargement [7,13,17,37], and the presence of fluiddebris levels within small cystic structures, around periphery of
© 2012 Informa UK, Ltd.
the ovary, is greatly suggestive of torsion of normal ovary, this
feature is presented in 13–45% of cases [13,17,36,37].
Color Doppler diagnostic contribution remains controversial
because of the dual blood supply to the ovary, thus the presence
of vascular flow to the ovary does not exclude torsion moreover,
intermittent torsion can lead to normal flow if the adnexa are not
twisted at that moment [5,7,14,36,37]. Studies report the absence
of Doppler flow in torted ovaries from 38 to 62% [36–38] and
Linam et al. [38] in their retrospective case-control study observe
the absence of doppler flow also in 1/3 of controls. The size and
the weight of ovarian lesions, specially of mature cystic teratoma,
are implicated in promoting torsion [1,5]. Oltmann et al. [7]
observe 83% of torsed ovaries have a US measurement of 5 cm
or larger while Rousseau et al. [13] observed only torsions under
15 cm, because large tumors are quite fixed, enclosed in the pelvis.
The same occurs for torsion in a malignant pathology, this is less
frequent because the tumor creates inflammation and adhesions to surrounding tissues reducing mobility and consequently
torsion [5,17,20]. Therefore, in pediatric age, the risk of malignant
ovarian neoplasm associated with torsion ranges from 2% to 6%
[7,20,21,32,39]. Because of the acute symptoms, CT and RM are
performed in doubtful cases only and their common imaging
features for ovarian torsion are enlarged adnexa or evidence for
adnexal mass, evidence of vascular congestion, ascites, tubal
thickening and uterine deviation to the twisted side [40,41]. In
emergency, levels of tumor markers such as β-HCG, α-FP, CA-125,
LDH are not routinely analyzed. The literature reports cases of
ovarian torsion with increase of tumor marker in presence not
only of malignant but also benign neoplasm [42,43]. Savic et al.
[20] reported a series of pediatric ovarian torsion and a review of
literature [32] with increase of LDH, β-HCG, αFP, CA-125 in 7
malignant germ cell tumors, increase of CA-125 in the presence
of 5 benign neoplasms and 3 non-neoplastic lesions. McCarthy
et al. [44] reported a case of a 6-year-old girl with ovarian torsion
in presence of increased CA-125 where the pathological diagnosis
was ovarian necrotic cellular debris. Takeda et al. [25] presented
the case of a 17-year-old girl with dysgerminoma complicated by
ovarian torsion and increase of LDH and β-HCG. We observed a
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4 C. Spinelli et al.
case of ovarian benign mature teratoma complicated by torsion
in association with increased α-FP. This finding suggests to be
cautious in performing a radical surgery in presence of elevated
tumor markers.
In the past concern for pulmonary embolism has induced to practice radical surgery but the literature shows only two adult cases of
pulmonary embolism, both occurred after salpingo-oophorectomy
without detorsion [19,45]. Whereas, in pediatric age there was only
one case, reported in a 16-year-old patient, of the right common iliac
vein thrombosed after left ovarian detorsion and cystectomy [46].
In medical literature, the standard procedure for many years
has been the removal of the twisted ovary, but our statistical study
shows that conservative treatment is slowly increasing from 28%
to 45% in the last 20 years. This is an important finding because it
reflects the greater interest in conservative surgery.
In ovarian torsion, laparoscopy is the recommended surgical
approach if technically possible. It provides the benefit of first
intervention when the diagnosis is unclear, decreasing the diagnostic delay and increasing conservative surgery [5,7,17,27,47].
Laparoscopic approach has an overall figure of 23.5% in the
review of the literature. With reference to Garliner et al. [17]
when the twisted ovary is below 75 mm, the surgical approach
should be laparoscopy, given the usual benign nature of the tumor
under this size, contrariwise, laparotomy should be performed.
The presence of edema, inflammation, congestion and ischemia determines an enlargement in dimensions of the ovary
and an aspect called black-bluish. This aspect may confuse decision making intraoperatively, resulting in a more aggressive use
of oophorectomy [21,48]. Most recent studies have shown that
there is no valid clinical method at hand predicting the viability
of the ovary and that the black-bluish macroscopic appearance
of the ovary is not a true indication of the degree of ischemia
[1,11,14,16,21]. Taskin et al. [49] in their study analyzed a rodent
model of ovarian torsion and performing histological analysis of
all black-bluish ovary they have concluded that adnexal integrity
is not correlated with gross ischaemic appearance. To obtain
information on the viability of ovarian tissue and to exclude the
presence of necrosis, it would be useful perform an intraoperative
frozen section analysis. Moreover, it is demonstrated that a blackbluish ovary, which does not change its color during operation,
is no evidence for a necrosis, and recovery is still likely to occur
[1,2,5,11,16–18,21]. In particular Celik et al. [11] reached 92% of
adnexal functional integrity, shown by ultrasonography follicle
growth. To decrease ovarian intracapsular pressure and facilitate
ovarian reperfusion and recovery, after untwisting the ovary,
some authors proposed ovarian bivalving [13,48], whereas others
do not agree on this procedure, because it could appear excessive
on an ovary already insulted by torsion [17]. Svensson et al. [9]
describe additional hyperbaric oxygen therapy which increases
the tissue oxygen tension, increases perfusion in injured tissue
and improves function of leukocytes with general anti-inflammatory effects. However, on previously normal ovaries complicated
by torsion, conservative management consists in detorsion alone,
even if they present severe ischemic-hemorrhages, without no
necrosis yet. After conservative treatment a clinical and a sonographic follow-up permit to observe two possible evolutions: the
ovary can retrieve its functional integrity by follicular presence,
with back to normal size or not, or, unfortunately, it can become
atrophic [11,14,16]. In their study, Wang et al. [39] observe an
ovarian recovery with normal size and normal follicular development in 33/35 (94.3%) cases treated conservatively while 2/35
cases (5.7%) become atrophic.
When cystic masses are diagnosed, detorsion of the adnexa
with synchronous cystectomy can be performed [1,17,33].
Otherwise it is possible to realize detorsion alone with surveillance in order to observe the evolution of the lesion and in case of
its persistence or enlargement in size practice a second look [5].
In presence of a solid or heterogeneous mass it is necessary,
after detorsion, to define if there is an underlying neoplasm [7]
and for this reason some authors suggest the use of intraoperative frozen section [39,50]. When a malignant lesion is diagnosed, staging is realized and an appropriate surgical procedure
can be adopted [5]. In case of benign lesions synchronous
tumorectomy can be performed but this procedure is technically difficult and it may cause further insult to the remaining
ovarian tissue with partial or complete involution of the
ovary [17,18,33]. Therefore it can be useful to practice detorsion alone with subsequent surveillance. Different authors
[11,14,16–18,21,33,51] suggest re-examining these patients
from 1 to 8 weeks after the acute episode, using ultrasonography and tumor marker levels because the edema and inflammation typically resolve and, at that time, ovarian tumorectomy
can be performed in a second look [13].
As to oophoropexy, this practice is proposed in order to prevent
recurrence of ipsilateral or contralateral adnexal torsion. Studies
show a risk of asynchronous bilateral ovarian torsion from 5%
to 13% [13–15,17]. This risk is higher if the first episode occurs
on the left side and on an ovary without any pathology [14]. In
fact, the left ovary has a lower frequency of torsion because of the
presence of the sigmoid colon which limits mobility [5–8,13,37].
In our review of literature we observed a frequency of 7.2%.
Oophoropexy is achieved using a non-resorbable swaged suture
and by fixing the ovary to the lateral part of the pelvic wall; to the
posterior wall of the uterus; to the posterior peritoneum just below
the bifurcation of the common iliac vessels [5,17]. Otherwise it is
possible to use the procedure of uterus ovarian ligament plication
which provides the means for shortening the uterus-ovarian ligament and thus reduces ovarian laxity [5,15]. Possible risks of this
procedure may include adherence and disturbance of the anatomic
tubo-ovarian relationship with displacement of the ovary from
the fallopian tube and subsequent infertility [12,15,33]. Because
no randomized, double–blind prospective studies, exist to solve
the question of the success of the pexy and its impact on future
fertility, the use of oophoropexy is controversial and not generally recommended for routine use [7,16]. Therefore, only selected
patients may benefit from pexy: those undergoing pelvic radiation for the treatment of malignancy, those presenting bilateral
torsion or recurrent ipsilateral torsion and when torsion occurs
on an ovary with a malformed or excessively long utero-ovarian
ligament [5,7,16].
In conclusion, the conservative surgical treatment of ovarian
torsion in children and adolescents, as evidenced in our study,
requires a specific knowledge of the physiopathology as well
as clinical and diagnostic aspects of the condition. In order to
maximize ovarian salvage it is necessary to perform diagnosis
and therapy as soon as possible. The laparoscopic approach
practiced in emergency, allows to reduce diagnostic delays.
The correct surgical procedure should be decided after ovarian
detorsion and only after intraoperative histopathological characterization of the lesion, especially in presence of solid or
mixed imaging.
Declaration of Interest: The authors report no declaration of
interest.
Gynecological Endocrinology
Surgery for ovarian torsion 5
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