# Ovarian Torsion in Prepubertal Girls: Clinical Characteristics, Biological and Radiological Features, Recurrence Rate

Coralie Defert, Audrey Cartault, Aurore Haffreingue, Pauline Clermidi, Chloé Lefébure, Adèle Olland, Mathilde Glenisson, Thomas Deleforterie, Agate Bourg, Pierre-Louis Vérot, et al.

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## To cite this version:

Coralie Defert, Audrey Cartault, Aurore Haffreingue, Pauline Clermidi, Chloé Lefébure, et al. Ovarian Torsion in Prepubertal Girls: Clinical Characteristics, Biological and Radiological Features, Recurrence Rate. Journal of Pediatric Surgery, 2025, 60 (6), pp.162317. 10.1016/j.jpedsurg.2025.162317. hal-05029458

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# Ovarian Torsion in Prepubertal Girls: Clinical Characteristics, Biological and Radiological Features, Reccurrency Rate☆

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Coralie Defert a, *, Audrey Cartault b, Aurore Haffreingue c, Pauline Clermidi d,
Chloé Lefébure e, Adèle Olland f, Mathilde Glenisson g, Thomas Deleforterie h,
Agate Bourg i, Pierre-Louis Vérot j, Elodie Haraux k, Marie Bousquet l, Françoise Schmitt m,
Yannis Bonnin n, Mélina Bourezma o, Charlène Messelod p, Manon Zislin q, Olivier Hild r,
Jean Breaud s, Alexis Belgacem t, Hélène François-Coridon u, Marie Bey v,
Sandy Jochault-Ritz w, Alexis Lubet x, Aurélien Scalabre y, Ianis Cousin z, Morgane Péré aa,
Estelle Le Pabic ab, Alexis P. Arnaud ac

## ARTICLE INFO

### Article history:

Received 12 December 2024

Received in revised form

5 February 2025

Accepted 30 March 2025

## ABSTRACT

**Introduction:** The diagnosis of ovarian torsion is made with delay among pre-pubertal girls and the management after the surgical detorsion is poorly codified. We interested in the French experience during the last two decades.

**Methods:** Retrospective study in French pediatric surgery centers from January 2000 to December 2022 concerning girls who presented with at least 1 episode of ovarian torsion in the prepubertal period. Data

<footnote>a Department of Pediatric Surgery, University Hospital of Nantes, France</footnote>

<footnote>b Department of Pediatric Gynecology and Endocrinology, University Hospital of Toulouse, France</footnote>

<footnote>c Department of Pediatric Surgery, University Hospital of Caen, France</footnote>

<footnote>d Department of Pediatric Surgery, Armand Trousseau Children's University Hospital, Paris, France</footnote>

<footnote>e Department of Pediatric Surgery, Necker-Enfants Malades, Paris, France</footnote>

<footnote>f Department of Pediatric Surgery, Jeanne de Flandre Hospital, Lille, France</footnote>

<footnote>g Department of Pediatric Surgery, Robert Debré Hospital, Paris, France</footnote>

<footnote>h Department of Pediatric Surgery, University Hospital of Bordeaux, France</footnote>

<footnote>i Department of Pediatric Surgery, University Hospital of Poitiers, France</footnote>

<footnote>j Department of Pediatric Surgery, University Hospital of Grenoble, France</footnote>

<footnote>k Department of Pediatric Surgery, University Hospital of Amiens, France</footnote>

<footnote>l Department of Pediatric Surgery, University Hospital of Tours, France</footnote>

<footnote>m Department of Pediatric Surgery, University Hospital of Angers, France</footnote>

<footnote>n Department of Pediatric Surgery, Lapeyronie University Hospital, Montpellier, France</footnote>

<footnote>o Department of Pediatric Surgery, University Hospital of Lyon, France</footnote>

<footnote>p Department of Pediatric Surgery, University Hospital of Reims, France</footnote>

<footnote>q Department of Pediatric Surgery, University Hospital of Strasbourg, France</footnote>

<footnote>r Department of Pediatric Surgery, University Hospital of Besançon, France</footnote>

<footnote>s Department of Pediatric Surgery, University Hospital of Nice, France</footnote>

<footnote>t Department of Pediatric Surgery, University Hospital of Limoges, France</footnote>

<footnote>u Department of Pediatric Surgery, University Hospital of Martinique, Fort-de-France, France</footnote>

<footnote>v Department of Pediatric Surgery, Hospital of Saint-Brieuc, France</footnote>

<footnote>w Department of Pediatric Surgery, Hospital of Colmar, France</footnote>

<footnote>x Department of Pediatric Surgery, University Hospital of Rouen, France</footnote>

<footnote>y Department of Pediatric Surgery, University Hospital of Saint-Etienne, France</footnote>

<footnote>z Department of Pediatric Surgery, University Hospital of Brest, France</footnote>

<footnote>aa Plateforme de Méthodologie et Biostatistique, CHU Nantes, France</footnote>

<footnote>ab CIC-1414, INSERM, CHU Rennes, France</footnote>

<footnote>ac Department of Pediatric Surgery, University Hospital of Rennes, France</footnote>

<footnote>Abbreviations: AXR, Abdominal X-ray; FP, alpha-Fetoprotein; CA 19-9, cancer antigen 19-9; CA 125, cancer antigen 125; CT-scan, computed tomography; HCG, human chorionic gonatrophin; LDH, lactate dehydrogenase; MRI, magnetic resonance imaging; PP, prepubertal.</footnote>

<footnote>* On behalf of all co-authors, I certify hereby that: all authors have made a substantial contribution to the information or material submitted for publication. All authors have read and approved the manuscript. No author has direct or indirect commercial financial incentive associated with the publication of the article.</footnote>

<footnote>* Corresponding author. 7quai Moncousu, 44000 NANTES, France. Tel.: +33 0609136243.</footnote>

<footnote>E-mail address: coralie.defert@chu-nantes.fr (C. Defert).</footnote>
**Keywords:**
Ovarian torsion
Children
Prepubertal
Reccurrent torsion

collected included patient history, symptomatology, biological and imaging assessment at first episode, emergency surgery, follow-up including recurrence.

**Results:** Thirty centers participated and we included 502 girls diagnosed with ovarian torsion during a surgical procedure performed due to abdominal pain (with or without ovarian mass). The girls had a mean age of 7.9 years (±2.8) and a median age of 8.3 years (Q1 5.97; Q3 10.12) at the time of the first episode of torsion. Nausea or vomiting was present in 71 % of cases. Fever was present in 23 % of cases and was more displayed 24 h after the onset of abdominal pain (p < 0.0001). Mean follow-up was 2.1 (±2.61) years. Only 42 out of 142 (30 %) girls with enlarged ovaries (>97th percentile) were referred to the endocrinologist to assess the existence of hormonal anomalies. Of the 482 girls without oophoropexy after the first episode of torsion, 71 (14.7 %) experienced at least one recurrence. Among them: 10 (7.5 %) had an ovarian mass and 42 (55 %) enlarged ovaries.

**Conclusion:** Symptoms of ovarian torsion in pre-pubertal girls are not specific and clinicians should be aware of this insidious presentation in this group. These girls should be systematically referred to endocrinologists.

© 2025 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license

(http://creativecommons.org/licenses/by/4.0/).

# 1. Introduction

The torsion of the ovary depicts what actually corresponds to the twist of the ovarian artery coursing through the suspensory ligament of the ovary. The ovarian artery originates posteriorly from the abdominal aorta and gives branches to the Fallopian tube. When the ovary flips, it creates a twist of this main artery, also dragging along the infundibulum or the entire adnexa. Rarely, it leads to the torsion of the utero-ovarian ligament alone (adjacent to the ascending branch of the uterine artery, which anastomoses with the ovarian artery), but in this case, it spares the Fallopian tube.

Ovarian torsion is less common in prepubertal (PP) girls than in adolescents. Because of this lower incidence, diagnosis is often delayed at the first episode [1]. PP girls are less likely to show cystic ovaries or tumor [2]. The risk of recurrence is greater in prepubescent girls than in adolescents [3].

The diagnosis of ovarian torsion is difficult because symptoms are nonspecific in PP girls [4]. This condition is poorly described among non-pubescent girls. We wanted to review the characteristics of concerned girls during this life stage, regarding their history and clinical presentation. Our study was part of a quality improvement project in our country to improve the management of ovarian torsion(s) in PP girls. The main outcome was the incidence of at least another ovarian torsion after a first episode that occurred during the prepubertal period, assessed with and without ovariectomy after the first episode of torsion.

# 2. Material and methods

This retrospective study in French departments of pediatric surgery included non-pubescent girls under 16 years of age who had at least one ovarian torsion between January 2000 and December 2022. Ovarian torsion comprised torsion of the ovary alone or of the entire adnexa. Diagnosis was made during a surgical procedure (laparoscopy or laparotomy) performed because of abdominal pain ± suspicion of torsion on imaging ± pelvic mass. An enlarged ovary was defined as having a volume greater than the 97th percentile [5]. The recurrence was defined as another episode of ovarian torsion, whatever the side affected.

Exclusion criteria were: mini-puberty (infants under 2 years of age) [6] or puberty (menarche occurring less than 2 years after the first episode of torsion), sonographic signs of estrogenic impregnation on the first US-scan (uterine height greater than 3.5 cm AND thickening of the body with a body/neck ratio greater than 1 OR

visibility of an echogenic cavity line over the entire uterine height) [7], girls over 10 years old whom date of menarche is unknown OR without any sonographic signs ruling out estrogenic impregnation at the time of the first torsion, known precocious puberty or discovered during etiological work-up after ovarian torsion; McCune-Albright syndrome, isolated torsion of the Fallopian tube or para-ovarian cyst without ovarian distress.

Collected data referred to: patient history (including ovarian transposition, abdominal surgery, ovarian torsion in first-degree relatives), symptoms during the first episode of torsion (duration and location of abdominal pain, vomiting, fever), imaging and laboratory work-up during the first episode of torsion, emergency surgery (side, route of access, intraoperative findings, ovariectomy, oophoropexy with details about the technique and the use of absorbable suture), etiological assessment (endocrinologist opinion, imaging and laboratory work-up), echo-clinical follow-up (ovary size at the time of the post-operative consultation and last follow-up, age at menarche, pregnancies), recurrence of ovarian torsion: episode of torsion occurring after the first detorsion whatever side (date, surgery with the same items as described above).

Data were collected between March 2022 and June 2023 in voluntary French departments of pediatric surgery and transmitted anonymized before analysis, after approval by our Institutional Review Board (approval 22.59). A descriptive analysis of the data was carried out globally and by group. This consisted in giving estimates in terms of numbers and percentages (rounded to the nearest unit when >1) for qualitative variables, and in terms of means, standard deviation, quartiles, minimum and maximum for quantitative variables. For the analysis of the primary endpoint, delay was defined as the time between the 1st torsion and appearance of the 2nd torsion. The cumulative risk was estimated using the Kaplan-Meier method. A McNemar-Bowker test was performed to study laterality between 1st and 2nd torsion. All statistical tests were performed with a significance level of 0.05. Statistical analyses were performed using the SAS software (version 9.4; SAS Institute, Cary, NC, USA).

# 3. Results

## 3.1. Patient demographics

We conducted the study at 28 tertiary centers and two secondary centers. We included 502 girls. Among the 90 patients excluded, 60 had sonographic signs of estrogenic impregnation, 4
had precocious puberty, 10 and 3 had respectively isolated Fallopi- an tube and para-ovarian cyst torsion, 3 were lost to follow-up, and 10 had too many missing data. Fifty-two girls (10 %) had a relevant medical history (Table 1). No one had an ovarian trans- position. Surgical history was remarkable in 15 girls (3 %) and included appendicular peritonitis (1 case), uncomplicated appendi- citis (2), inguinal hernia repair (5) homolateral to the first ovarian torsion, nephrectomy for nephroblastoma (2), duodenal atresia complicated by intestinal obstruction (1), ovarian detorsion before 2 years of age (1), ovarian sparing surgery for mature teratoma (1), contralateral oophorectomy for mature teratoma (1) and for exci- sion of an antenatal cyst without torsion (1). There was a history of ovarian torsion in the mother in 6 cases (1.2 %) and in one twin sister before puberty. The mother's bilateral ovarian dystrophy was reported in one case. Two mothers had polycystic ovary syndrome, and another had a mature ovarian teratoma similar to her daughter.

## 3.2. Clinical presentation (Fig. 1)

The girls had a mean age of 7.9 years (±2.8) and a median age of 8.3 years (5.97; 10.12) at the time of the first episode of torsion. Abdominal pain was a constant symptom generalized in 260 cases (40 %), homolateral to the torsion in 269 (54 %), and contralateral in 16 (3 %). In 17 cases (3 %), it was unspecified. Nausea or vomiting was present in 358 patients (71 %) and unspecified in 45 patients (9 %). Fever was present in 105 (23 %) patients, absent in 345 pa- tients (76 %) and not reported in 8 patients (1 %). Fever was more frequently displayed by girls when they consulted after 24 h following the onset of abdominal pain (p < 0.0001) and it was significantly associated with necrotic ovary intraoperatively (p < 0.01).

<table><caption>**Table 1**
Detailed medical history of 52 girls.</caption><tr><td>GYN</td><td>Ovarian cyst diagnosed antenatally with complete regression (5)<br/>Known ovarian cyst (5)<br/>Vulvar angioma (1)</td></tr><tr><td>SYS</td><td>Diabetes type 1 (2)<br/>Polyarthritis (1)<br/>Connectivitis (1)<br/>Henoch-Schonlein purpura (1)<br/>Unexplained fever (1)<br/>Kawasaki + juvenile arthritis (1)</td></tr><tr><td>SD</td><td>Intestinal malrotation + solitary kidney (1)<br/>Bardet-Biedl syndrom (1)<br/>X triploidy (1)<br/>Omphalocele (1)<br/>Turner syndrom (1)</td></tr><tr><td>NEUR</td><td>Epilepsia (1)<br/>Migraine (2)<br/>Guillain-Barre syndrom (2)</td></tr><tr><td>CARD</td><td>Interatrial communication (2)<br/>Interventricular communication (1)</td></tr><tr><td>PNM</td><td>Asthma (5)<br/>Pulmonary sequestration (1)<br/>Sleep apnea (1)</td></tr><tr><td>GASTRO</td><td>Constipation (1)<br/>Cystic lymphangioma (1)<br/>Biliary lithiasis (1)<br/>Auto-immune hepatitis (1)</td></tr><tr><td>DER</td><td>Atopic dermatitis (1)<br/>Congenital naevus (1)<br/>Peri-anal condyloma (1)</td></tr><tr><td>ENT</td><td>Chronic infections (3)<br/>Neck lymphangiome (1)</td></tr><tr><td>OTHERS</td><td>Allergy (2)<br/>Von Willebrand disease (1)</td></tr></table>

GYN: gynecology, SYS: systemic diseases, SD: syndrome, NEUR: neurology, CARD: cardiology, PNM: pneumology, GASTRO: gastroenterology, DER: dermatology, ENT: ear neck and throat.

## 3.3. Biological features

- inflammatory markers

White cell counts and C-Reactive Protein levels were retrieved from the files of 15 cases. Torsion was diagnosed at least 24 h after the onset of pain in 13 patients who also had fever. One patient had inflammatory syndrome, but no fever after 24 h. One case had in- flammatory syndrome but no fever and the pain was lasting for 6–12 h.

- tumor markers (Table 2a)

Tumor markers were sampled in 296 cases (59 %). Germ cell tumor markers alone (αFP, HCG) were concerned in 148 cases (29 %). Notice that HCG and αFP were measured alone in 5 and 6 cases respectively. In 5 cases (1 %), tumor markers were collected but did not include αFP or HCG: estradiol alone (1 case), LDH alone (2), estradiol + testosterone + inhibin (1), and estradiol + testosterone + inhibin + AMH (1). Epithelial tumor markers (CA125 and/or CA 19-9) were assayed in 65 cases (13 %) and were always associated with germ cell tumor markers, and variably with estradiol, testosterone, AMH, inhibin, and LDH. Thir- ty-six patients (7 %) had at least one abnormally elevated tumor marker (excluding abnormal AMH alone). There were no false positive results.

- pathology report (Table 2b)

Pathological analysis revealed 153 tumors (30 %). αFP was abnormal in one out of four cases of immature teratomas (12 ng/ml) and in 1 patient with mucinous cystadenoma (11 ng/ml). A patient with undifferentiated SCST had inhibin level of 410 pg/ml, normal HCG level, and αFP level of 39 ng/ml. The patients with the gran- ulosa tumor and the dysgerminoma had no pre-operative tumour marker sampling.

## 3.4. Radiological features

The diagnosis was suspected or confirmed by ultrasound in 363 patients (72 %). In 10 cases (2 %), emergency imaging modalities were not found. No imaging was performed in 2 cases (<1 %). Abdominal X-ray alone (AXR) was performed in 2 cases (<1 %), ultrasound and AXR or CT-scan alone in 5 cases respectively (1 %), ultrasound + CT-scan in 71 cases (14.0 %), ultrasound + MRI in 48 cases (9 %), ultrasound + CT-scan + MRI in 8 cases (1 %). Enlarged ovaries were identified in 154/502 girls (30 %). Surgery was also performed if the radiologist did not clearly rule out a torsion.

## 3.5. Surgical procedure

Surgery was performed laparoscopically in 362 patients (71 %), by laparotomy in 72 patients (15 %), and by laparoscopy converted to open in 70 cases (14 %). Conversion was associated with oo- phorectomy or tumor removal at the same time in 67/70 cases (96 %).

The torsion was right-sided in 310 cases (61.9 %), left-sided in 189 cases (37.7 %), and bilateral in 2 cases (0.4 %). Intraoperative findings were reported in 411 cases (82 %): 42 congestive ovaries (8 %), 174 ischemic ovaries (35 %), and 128 necrotic ovaries (26 %). A mass was described in 67 cases (13 %), regardless of the condition of the ovary. Peritoneal fluid cytological analysis was more frequently performed in the presence of a mass according to the surgeon's findings (47/60 cases (78 %), undetermined in 7 cases and unre- quested in 6 cases; p < 0.0003).
<figure><img src="image_3.png" /><figcaption>**Fig. 1.** Distribution of girls (%) according to delay for suspected diagnosis of ovarian torsion after the onset of abdominal pain (n = 486). The suspicion was based on imaging finding or clinical exam.</figcaption></figure>

<table><caption>**Table 2**
Tumors.</caption><thead><tr><th colspan="9">a. Sampling frequency for tumoral markers.</th></tr><tr><th></th><th>hCG</th><th>αFP</th><th>Estr.</th><th>Testo.</th><th>AMH</th><th>inhibin</th><th>LDH</th><th>CA 19-9</th><th>CA 125</th></tr></thead><tbody><tr><td>Number of cases sampled n = 296 (100 %)</td><td>154 (52)</td><td>153 (51)</td><td>41 (14)</td><td>24 (8)</td><td>31 (10)</td><td>47 (16)</td><td>38 (13)</td><td>31 (10)</td><td>40 (13)</td></tr><tr><td colspan="10">b. Pathological reports of the 153 tumours (30 %). For 23 cases (4 %) no conclusion was possible because of the necrosis of the sample.</td></tr><tr><td><strong>Benign</strong> 120 (24 %)</td><td>Mature teratoma (98, 19 %)</td><td>Serous cystadenoma (8, 2 %)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Borderline</strong> 2 (&lt;1 %)</td><td>Mucinous cystadenoma (2)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td><strong>Malignant</strong> 10 (2 %)</td><td>Immature teratoma (4, 1 %)</td><td>Sex cord-stromal tumors (granulosa) (3)</td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr></tbody></table>

Twenty patients (4 %) underwent oophoropexy at the same time: 14 (3 %) involved the homolateral ovary and the contralateral ovary was fixed in 6 cases (1 %) following oophorectomy (for tumor in 3 cases). No bilateral oophoropexy was performed. Analysis comparing efficiency of oophoropexy according to the technique and the material used was impossible because of the heterogeneity of techniques.

Other procedures were performed at the same time in 193 cases (38 %): 136 oophorectomies (27 %), 20 lumpectomies (4 %), 14 lumpectomies (cystic) (2 %), 9 punctures of an ovarian cystic mass (2 %), 7 appendectomies (1 %), 4 biopsies (0.8 %), 1 homolateral ovarian sparing surgery + contralateral ovary biopsy, 1 oophorectomy + contralateral ovarian sparing surgery, and 1 resection of the suspensory ligament of the ovary.

### 3.6. Follow-up

The first postoperative consultation was attended by 430 girls (85 %) and occurred on an average of 41 (±20) days after surgery. The mean follow-up duration with systematic consultation was 2.1 (±2.61) years, and the median follow-up duration was 1 year (Q1 0.33; Q3 2.80). The mean follow-up period since the first episode of

torsion was 10 (±4.6) years and the median was 8 years (Q1 5; Q3 12). Sixty-seven girls (13 %) were referred to an endocrinologist after their first episode of torsion. Even among the 142 girls with enlarged ovaries (>97th percentile), only 42 (30 %) were referred to an endocrinologist. The median and mean ages at menarche were 13 (Q1 12; Q3 13) and 12.5 (±1) years, respectively.

### 3.7. Recurrent ovarian torsion(s) (Fig. 2)

Of the 482 girls without oophoropexy after the first episode of torsion, 71 (14.5 %) experienced at least one recurrence. Among these girls with repeated torsions: 10 (7.5 %) had an ovarian mass and 42 (55 %) enlarged ovaries. Eighteen (25 %) patients had insufficient or no ultrasound measurements to determine the volume of the ovaries. The side affected during the first recurrence was independent of the side affected during the first episode (p < 0.05). Recurrence rate after the first episode for girls who never had oophoropexy or ovariectomy was 18 % (Fig. 3a). If there was an ovariectomy and no oophoropexy, the rate of first recurrence was 7 % but it reached 10 % if we did not take into account ovariectomies for tumour (Fig. 3b). This risk increased after each new episode of torsion if no fixation was performed during the procedure of detorsion (homolateral or bilateral).
<figure><img src="image_4.png" /><figcaption>**Fig. 2.** Survival curve expressing the time between a) the first episode of torsion and the first recurrence b) the first and the second recurrence. Four years after the first torsion, 93 % (70/75) had already displayed their first recurrence. After the first recurrence, almost 100 % (19/20) of the girls displayed the following recurrence (third episode of torsion) within 2 years. The period between each new episode afterwards was always inferior or equal to 2 years (figures not shown).</figcaption></figure>

<figure><img src="image_5.png" /><figcaption>**Fig. 3.** Recurrence rate. a. Flow-chart displaying the cumulated recurrence rate for girls who underwent an ovariectomy after the first episode of torsion. After each episode of torsion, girls with oophoropexy or ovariectomy were excluded. b. Flow-chart displaying the cumulated recurrence rate for girls without ovariectomy who never underwent oophoropexy on any of their ovary. After each episode of torsion, girls with oophoropexy were excluded.</figcaption></figure>

# 4. Discussion

The extensive dataset obtained for a low-prevalence condition from a national study enabled us to emphasize points to improve the management of ovarian torsion in PP girls. For the first time, the rate of recurrence after a first episode of ovarian torsion in this population was reported (7 % if ovariectomy, 18 % without ovariectomy).

This large-scale study was designed with very selective exclusion criteria because we also aimed at drawing hypothesis on the

pathophysiology of ovarian torsion among prepubescent girls from the analysis of descriptive data. Regarding clinical history, the prevalence of appendicitis (3) was lower in our cohort than in a recent systematic review based on population based studies [8]. We suggest that inflammation due to peritonitis or adhesions from the surgery itself could diminish ovarian motility. The prevalence of autoimmune diseases, which are rare in infants, was surprisingly high (Table 1). Ovarian torsion after transposition is extremely rare in adults [9] and has never been described in children. Family history of ovarian torsion, except from the mother and twin sister, is
probably not either a risk factor. Furthermore, we have never dealt with ovarian torsion after transposition in our respective experiences.

The localization of abdominal pain was not specific. It was impossible to describe the first pain reported in the emergency department because of the lack of data. Literature has shown that vomiting is a good clinical sign of gonad torsion (67 %) [10] similarly to our study (71 %). It witnesses an intense pain due to ischemia causing a vagal reflex. Diagnosis was made after 12 h in 85 % of girls, and only 5 % of diagnoses were made before 6 h. Patient transfer to a center with pediatric surgeons was not the main reason for this delay. Constipation was one of the diagnoses often suggested at first. Imaging was then carried out because the pain persisted after the patient returned home. The ovary's resistance to ischemia is said to be greater than that of the testis, and a blue-black ovary intraoperatively is not synonymous with necrosis, which has led to the recommendation that systematic oophorectomy should no longer be performed even in the presence of this appearance [5]. After 24 h of evolution, the symptomatology (fever and inflammatory syndrome) can mislead practitioners and mimic appendicitis. That is why ovarian torsion should be ruled out during a surgical procedure performed for appendicitis if the appendix is healthy. Ultrasound-scan is a simple, easily accessible and non-irradiant exam that may be very helpful to distinguish common benign conditions that are diagnostics of exclusion (mesenteric adenitis, constipation) and anomaly on the ovary. Indeed, 90 % of girls before 10 years of age have an ovary size inferior to 2.5 cm⁷. An ovary measuring twice this size may be suspected of torsion. Moreover, in the case of a non-pubescent girl with no history of constipation and no scanographic signs of adenitis, the diagnosis of ovarian torsion should be discussed. An ovarian tumour was found in 1 case out of three torsions among prepubescent girls. This rate is lower than that in cohorts gathering girls from birth to teenage-hood [11,12]. Extensive sampling of tumor markers did not prevent two cases of malignant tumors from being untested. Screening of tumour markers was also very heterogeneous in our study. There are namely no guidelines regarding tumour markers in the management of an ovarian masses in children, except for HCG and α-FP for germinal tumors which are the most frequent in children. CA-125 is recommended in adults and is often associated with HCG and α-FP in children [13] but it is a marker of epithelial ovarian cancer which is extremely rare in infants. Though, it can be high in very large serous cystadenomas [14]. Further studies are needed to evaluate the tumor markers that should be sampled in an emergency if a mass is suspected to be the cause of ovarian torsion. Biopsy, puncture or appendectomy are not recommended in the management of ovarian tumour [15], whether before or after detorsion.

In prepubescent girls, plication of the utero-ovarian ligament or fixation of the adnexa to the pelvic sidewall are recommended if indicated [16]. The combination of these two techniques seems to reduce the risk of ovarian torsion after oophoropexy [17]. None of the patient in our study underwent plication of the utero-ovarian ligament. Among the girls who had a fixation to the sidewall, it was impossible to gather 2 girls who had the same number of stitches and the same type of thread used (absorbable or not). Procedures to prevent repeated ovarian torsions in young girls meet a few difficulties: the pelvis is a limited workspace and the ovary has not reached its final size but still, can be bulky especially due to edema and/or because it is enlarged.

The first recurrence rate of ovarian torsion without tumor (14.5 %), specifically among prepubescent girls and after mini-puberty (up to 2 years of age15) has never been published until

now. Ashwal et al. [18] reported a higher recurrence rate (18 %) however, most patients had ovarian cysts. Tasset et al. [4] had a similar rate, but the number of girls who did not undergo oophoropexy or ovariectomy was low. In other studies, recurrence rates are lower but the groups of patients studied encompassed infants, teenagers and women [19] or studies concerned ovarian torsion during pregnancy [20], after systematic oophoropexy or in groups with a large amount of ovariectomies [21–23]. The first ultrasound scan was not systematically performed by a pediatric radiologist. We questioned the entity of “normal ovary” because it was not rare that the volume jointly reported was not normal considering the age of the patient [5]. This could explain the underestimation of enlarged ovaries [24]. Indeed, if we exclude masses responsible for recurrence, at least 72 % (9/12.5 %) of the girls displaying recurrences had enlarged ovaries. There is no evidence that enlarged ovaries are always pathological but guidelines from Societies of Endocrinology [25] suggest to make a clinical assessment of the girls concerned and run lab tests exploring the hypothalamo-hypophyseal axis especially because ovarian enlargement with or without cyst is also a criteria accounting for Polycystic Ovarian Syndrom. It seems that most recurrences occur within 4 years after the first episode. Given the median age of the cohort (approximately 8 years), menarche or at least puberty could explain this decrease in recurrence. The underlying factors that may explain the sudden decrease in recurrence are unknown.

The main limitation of our study is obviously the lack of data linked to our interest in information that is collected inconsistently. To infer that there is still no point requesting for these data would be a mistake. On the contrary, we believe that the flaws in this retrospective study (3D-measurements of the ovary, assay of markers secreted by the main ovarian tumors in prepubertal girls, age of menarche, heterogenous techniques of oophoropexy sometimes not described in the literature) reflect the lack of knowledge and/or interest in the pathogenesis of ovarian torsion from the practitioners who manage these girls (pediatric surgeon, pediatricians, radiologists, endocrinologist). An exhaustive database would enable a comparative analysis to be carried out to identify risk factors and thus define preventive attitudes. A national prospective study has been implementing in France following the results of this study.

Ovarian torsion in prepubescent girls is an entity that should not be confonded with those occurring in females releasing estrogenic factors. This will enable to separate analysis focusing on this group to unravel the causes of torsion and the risk factors for recurrence. For better clinical assessment of these girls, every non-pubescent child displaying ovarian torsion should be sent to an endocrinologist.

## Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

## Acknowledgements

Acknowledgements to the following pediatric surgeons for providing data from patients managed in their respective centers: Pr Marc-David Leclair and Dr Sébastien Faraj, University Hospital of Nantes; Pr. Olivier Abbo, University Hospital of Toulouse; Pr. Florent Guérin, University Hospital of Bicêtre; Dr Armande Subayi, University Hospital of Lille; Dr Marie-Pierre Guibal, University Hospital of Montpellier; Dr Eva Mille, University Hospital of Marseille; Dr David Louis, University Hospital of Dijon.
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