Adnexal torsion in girls: Predictors and methods for surgical treatment. Case reports and review

Full Text

BACKGROUND

Adnexal torsion (AT) in girls occurs in 2.7%–4.9% of all patients with abdominal pain in a surgical hospital [1–3]. Modern methods of diagnosis and treatment allow for preoperative diagnosis and surgical care. However, the causes and definition of the scope of surgical treatment remain controversial.

This study aimed to analyze Russian and foreign publications on predictors of AT and surgical correction of torsion in children, based on our observations.

DESCRIPTION OF CLINICAL CASES

Video recordings of 20 laparoscopic surgeries performed for AT in girls aged 3–17 years at St. Vladimir’s Children’s City Clinical Hospital between 2017 and 2023 were analyzed retrospectively. Ultrasonography was used as the mandatory preoperative screening method of diagnosis performed according to the standard technique on the Voluson E8 device (Austria) using convex and linear transducers of 2–15 MHz. To optimize the image, the B-color mode with color Doppler mapping was used in most cases. Surgeries were performed using an endovideosupport system by Karl Storz (Germany), with a three-chip SLII high-resolution video camera with a block and standard set of instruments, including 5 and 10 mm trocars, mono and bipolar electrocoagulation instruments, scissors, forceps for grasping and dissection, and needle holder. Magnetic resonance imaging (MRI) was performed for postoperative diagnosis. A Toshiba device (Excelart Vantage Atlas-X, USA) with an actively protected magnet of 1.5 Tesla and a reconstructed image thickness of ≥1 mm was used. The study protocol involved using conventional MRI to image the abdominal and pelvic organs, and T1- and T2-weighted images were acquired in axial, sagittal, and frontal projections.

The table summarizes the causes of torsion and the number and types of surgical interventions.

 

Table. Etiology and types of operations for uterine torsion

Таблица. Этиология и виды операций при перекруте придатков матки

Surgery	Ovarian cysts	Paramesonephric cysts	Fixed lateroflexion	Unspecified	Number of patients
					n	%
Detorsion	2	–	–	–	2	10
Detorsion with fixation	5	–	5	2	12	60
Detorsion with resection	–	4	–	–	4	20
Detorsion with adnexectomy	–	–	1	–	1	5
Adnexectomy without detorsion	–	–	–	1	1	5
Total	7 (35%)	4 (20%)	6 (30%)	3 (15%)	20	100

 

Detorsion without fixation was performed when ovarian cysts >5 cm were detected. Children were then transferred to gynecologic departments for interval surgery. If the structure of the black appendage was disturbed during detorsion and fragmented when untwisted, adnexectomy was performed. In four observations of paramesonephral cysts, an isolated torsion of the fallopian tube was detected without any disturbance of ovarian blood flow. After detorsion, no blood flow restoration was detected in the fallopian tubes. In one case, the patient underwent cyst enucleation in the hope of restoring blood supply; however, this was not successful. All children underwent salpingectomy without ovarian fixation. Lateroflexion was detected in seven cases; however, the change in uterine angle was considered transient in only one case (Fig. 1).

 

Fig. 1. Adnexal torsion with transient lateroflexion of the uterus: a — adnexal torsion on the right; classical transient right-sided uterine lateroflexia caused by the mass effect; and b — condition after detorsion. The uterus is in a central position

Рис. 1. Перекрут придатков с транзиторной латерофлексией матки: а — перекрут придатков справа. «Классическая» транзиторная правосторонняя латерофлексия матки, вызванная масс эффектом (mass effect); b — состояние после деторсии. Матка в центральном положении

 

After detorsion, in six observations, the uterus maintained a fixed lateroflexion position, deviating from the conventional central axis to the left or right side. In addition to the increased ovarian mass and size, two main factors contribute to the development of torsion in uterine lateroflexion:

1. The lateral deviation of the uterus reduces the space of the ovarian fossa and prevents the ipsilateral gonad from descending into the pelvis (Fig. 2).

 

Fig. 2. Adnexal torsion with left-sided lateroflexion of the uterus: a — adnexal torsion on the left; b — the condition after detorsion; and the yellow line means conditional; c — the layout of the torsioned adnexal (arrow)

Рис. 2. Перекрут придатков при левосторонней латерофлексии матки: a — перекрут придатков слева; b — состояние после деторсии. Желтая линия — условная центральная ось; c — схема расположения торсированного придатка (указан стрелкой)

 

This positioning can result in the torsion of the altered or unaltered ovary because of physical strain, active peristalsis, or excessive gas.

2. The lateral deviation of the uterus increases the space in the ovarian fossa on the opposite side, which could potentially lead to torsion (Fig. 3).

 

Fig. 3. Adnexal torsion on the left: a — torsion of the “healthy” adnexa on the left. The arrow indicates the torsioned left ovary; b — right-sided uterine lateroflexia; the yellow line indicates the conditional central axis; and c — scheme of the formation of a free space in the pelvis (arrow)

Рис. 3. Перекрут придатков слева: a — перекрут «здоровых» придатков слева. Стрелкой указан торсированный левый яичник; b — правосторонняя латерофлексия матки. Желтая линия — условная центральная ось; c — схема образования свободного пространства в малом тазу (указано стрелками)

 

In the above observations, the ligamentous apparatus of the uterus and ovaries was used to unilaterally fix the appendages through plication.

Two observations of AT are of interest, in which the contralateral gonad was located over the uterus (Fig. 4). For this appendage location, bilateral fixation was performed after detorsion.

 

Fig. 4. Adnexal torsion on the right: a — the left ovary above the uterus (arrow); b — state after detorsion. The left ovary maintains its position. The right adnexa in the free abdominal cavity (arrow)

Рис. 4. Перекрут придатков справа: a — левый яичник над маткой (указан стрелкой); b — состояние после деторсии. Левый яичник сохраняет свое положение. Правый придаток в свободной брюшной полости (указан стрелкой)

 

The change in the angle of inclination may be associated with dysplasia of the ligamentous apparatus of the uterus or ovaries. This is indirectly confirmed by the detection of three inguinal hernias on the ipsilateral side in patients with lateroflexion and pelvic floor muscle development and/or pelvic adhesions (Fig. 5).

 

Fig. 5. Adnexal torsion on the left. Condition after detorsion. Left-sided lateroflexion of the uterus. The arrow indicates a left-sided inguinal hernia

Рис. 5. Перекрут левых придатков. Состояние после деторсии. Левосторонняя латерофлексия матки. Стрелкой указана левосторонняя паховая грыжа

 

In the analysis of the case histories of the patients, preoperative transabdominal ultrasonography showed the uterus deviating toward ovary torsion in one patient. Based on this data, we determined the position of the uterus in girls who underwent laparoscopic surgery for nongynecologic abdominal pathology. Consequently, left-sided lateroflexion of the uterus was detected in a 10-year-old girl who underwent surgery for destructive appendicitis (Fig. 6).

 

Fig. 6. Endoscopic view during revision of the pelvic organs. The arrow points to the left-sided lateroflexion of the uterus

Рис. 6. Эндоскопическая картина при ревизии органов малого таза. Стрелка указывает на левостороннюю латерофлексию матки

 

Postoperatively, transabdominal ultrasonography and MRI were performed to examine the pelvic organs. However, echography data did not provide any useful information. Conversely, MRI confirmed the presence of uterine lateroflexion (Fig. 7).

 

Fig. 7. Magnetic resonance tomography of the lower abdominal cavity. The uterus is in the anteflexio and retroversio position, with clear boundaries. The body is tilted to the left (arrow). The right ovary at the entrance to the pelvis (oval)

Рис. 7. Магнитно-резонансная томография нижнего одела брюшной полости. Матка в положении anteflexio, retroversio, с четкими границами, тело отклонено влево (стрелка). Правый яичник у входа в малый таз (овал)

 

This study has the limitations of a retrospective study. The small number of patients currently complicates the identification of uterine lateroflexion as a potential predictor of AT. Further study of this problem is necessary.

LITERATURE REVIEW

A systematic search was conducted in the PubMed, Scopus, eLibrary, and RSCI databases. In total, 47 references were analyzed, 58 articles were reviewed, and 39 publications that focused on the identification of predictors of AT in children and its methods of surgical treatment were selected.

Etiology

The etiology of AT is not fully understood; however, cystic formations (functional, retention, and paramesonephric) and tumors (benign and rarely malignant) of the uterine appendages are considered the main disease predictors [1–7]. According to R.M. Rocha and I.D.E.S. Barcelos [7], the main causes of AT from a large series of observations (360 patients) were dermoid cysts (36%), follicular cysts (16.1%), and corpus luteum cysts (9.9%). C. Spinelli et al. [6] reported the results of a histologic study involving 97 patients, and they identified functional cysts as one of the causes of AT, including the following: follicular (34.7%), simple (30.6%), corpus luteum (14.3%), serous (8.2%), and pseudocysts (6.2%). Dermoid cysts were detected in 25 (25.8%) patients. In addition, torsion of unchanged appendages was observed in 11 (11.3%) cases. In the systematic review of the literature on AT in the pediatric population with an average age of 11.6 years, O. Adeyemi-Fowode et al. [8] revealed that girls in the premenarchal period accounted for 43.4% of observations, whereas girls in the postmenarchal period accounted for 56.6%. The authors attribute the increased morbidity in adolescence to hormonal influences and the growth of the gonads, which leads to an increased frequency of physiologic and pathologic masses. Most studies have reported an association between AT and increased ovarian mass and size >5 cm. Paramesonephric cysts are considered a rare cause of AT, occurring in approximately 10% of cases. According to most experts, isolated fallopian tube torsion is almost always associated with a paratubal cyst or hydrosalpinx [8–11]. Ovarian malignancies are an even less frequent cause of ovarian torsion. In a pooled series of studies including 707 patients with AT, S.C. Oltmann et al. [12] found malignancy in only 1.8% of cases. According to various authors, the cause of AT was unidentified in 21%–46% of pediatric patients [8, 12]. The etiology of AT in the absence of cysts or neoplasms is unclear and may be due to the increased mobility of the appendages caused by elongated ovarian ligaments or a hyperelastic type of mesosalpinx or mesovarium. The relatively small size of the uterus in premenarchal girls may provide a suitable space for AT. Increased blood pressure in the veins of the neoplasm’s pedicle or the ovary is believed to play a role in AT development [8, 12, 13]. Dysplastic changes in the ligamentous apparatus of children, as pointed out by L.V. Adamyan et al. [3], may be an internal manifestation of AT.

Pathogenesis

Girls with AT experience changes in body position, physical exertion, increased intestinal peristalsis, and bladder overflow [2, 8, 12, 14]. Several authors have reported that right-sided AT is 1.5 times more common [4, 15, 16]. According to L. Darrell, the increased risk of right-sided torsion can be attributed to the larger space on the right side of the pelvis, which is filled with sigmoid colon, and the hypermobility of the cecum and ileum [17]. In addition, the author cited the work of S.J. Boley et al. [18] and highlighted the significant role of irreparable inguinal hernias in AT occurrence in girls. This was detected during hernioplasty in 27% of the cases [17].

Clinical presentation and diagnosis

The clinical presentation of AT is not dependent on the causative factors and is quite characteristic but not disease-specific [2, 5]. Symptoms resulting from AT can imitate destructive appendicitis, urinary tract infections, renal colic, gastroenteritis, or other causes of acute abdominal and pelvic pain. Transabdominal ultrasonography with Doppler imaging is the primary screening procedure for visualizing AT in children [2, 19]. Ultrasonography reveals an enlarged ovary with increased echogenicity, often accompanied by small peripheral cysts. In some cases, the ovary and uterus may be displaced to the same side. Doppler ultrasonography can detect blood flow disorders in the affected ovary, which is characterized by a whirlpool sign consisting of numerous concentric hypoechogenic rings resembling the shape of a target [21, 22]. However, the presence of blood supply on Doppler examination does not necessarily exclude AT because of the dual blood supply from the ovarian and uterine arteries and venous hemorrhage occurs before the arterial channel is damaged [3, 23]. Ultrasonography is also used postoperatively to monitor the recovery of the injured ovary [19]. Based on the literature, folliculogenesis is restored within 3 months to 3 years, as determined by echography [21, 24–27]. In addition to ultrasonography, recent publications have discussed the use of radiologic diagnostic methods such as multispiral computed tomography (MSCT) and MRI. For instance, S. Gounder et al. reported that in approximately half of the cases, MSCT and MRI detected uterine deviations to the side of the lesion, which, along with ovarian displacement (medialization), indicates AT [28, 29]. CT can detect ovarian teratomas with calcifications, which may cause AT. In addition, MSCT is useful in identifying other causes of abdominal pain, such as appendicitis or urinary system concretions, which can mimic ovarian torsion. However, A.V. Ngo et al. [23] do not recommend using MSCT for suspected ovarian torsion because of high doses of ionizing radiation and low cost-effectiveness compared with ultrasonography. MRI is not commonly used in cases of suspected acute ovarian torsion because of issues with availability, cost, and most importantly, the timing of the procedure, which is a crucial factor in preserving appendiceal viability [30]. However, as several studies have indicated, MRI is the preferred method for visualizing uterine appendiceal neoplasms that have resulted in torsion and can be performed after detorsion [21, 31].

These findings, along with the clinical presentation, necessitate the use of an invasive visualization method, which is confirmed by laparoscopy [2, 14, 32].

Treatment

Laparoscopic visualization of AT and detorsion does not pose a challenge [2]. However, the operating surgeon faces several challenging tasks. First, they must determine the viability of the organs involved because this determines the extent of the surgical intervention. Second, they must identify and eliminate the cause of torsion if possible. Finally, they must address appendage fixation. The available literature presents conflicting opinions.

Only a completely changed appendage should be removed. Organ viability is determined visually by its color. Viability is determined by blood flow restoration after untwisting. S.V. Parelkar et al. [33] distinguished four degrees of ischemia, ranging from a slightly discolored ovary to red, brown, and black. They described 10 observations of detorsions in which the ovaries were severely ischemic or necrotically altered at the time of surgery. However, subsequent sonograms revealed gonad preservation with follicle development in nine patients [33]. Dasgupta et al. (34) conducted a 20-year retrospective analysis of necrotic appendage preparations, defining a viability index based on the percentage of intact tissue identified (one for 0%, two for 1%–25%, three for 26%–75%, and four for >75%). At the time of surgery, ovaries described as “black” contained viable glandular tissue in 38%, and 21% of observations had an index of four. The American Association of Pediatric Surgeons and the Outcomes and Evidence-Based Practice Committee conducted a study to provide recommendations for optimizing the treatment of ovarian torsion. The authors concluded that appendiceal detorsion in pediatric patients without ovariectomy is strongly supported by compelling evidence because most of the rescued ovaries remain viable [34].

However, no consensus has been established on whether to remove cysts during detorsion. According to N. Smorgick et al. [35], pediatric patients can be divided into two groups: those with torsion of “pathologic” appendages (ovarian cysts or paramesonephric cysts) and those with torsion of “normal” appendages. In the first group, surgical treatment should include detorsion, cystectomy, fenestration, or cyst puncture, which reduces the risk of recurrent appendiceal torsion by 50%–75% [35]. However, performing cystectomy on ischemic, severely edematous, friable appendages may lead to further damage to the gonadal tissue and bleeding and require emergency ovariectomy. In such cases, only detorsion to preserve the ovaries should be considered, and cyst removal should be performed routinely [8, 27, 36].

Fixation of the uterine appendages is challenging. The literature describes several techniques of ovariopexy, including the fixation of the ovary to the lateral pelvic wall, plication of the sacrouterine and round ligaments, shortening the uterine ovarian ligament, and suturing the uterine ovarian ligament to the posterior uterus. However, according to E. Simsek et al. [37], ovarian fixation lacks standardization, and the optimal method of ovariopexy remains undefined. Furthermore, plication does not eliminate the risk of retorsion, which can reach 12% [8, 37, 38]. The article discussed theoretical risks associated with uterine appendage fixation, including potential obstruction of the ovary descending into the fossa during puberty, uterine blood supply impairment, fallopian tube function, or ovary–fallopian tube connection. These risk factors may lead to iatrogenic infertility and require in vitro fertilization [8]. According to L.L. Breech et al. [14], all complex issues must be discussed with the patients and parents, which justifies an interval procedure instead of ovariopexy during primary surgery. In addition, planned interventions after the acute ischemic manifestations have subsided provide better appendage fixation with the restoration of the normal anatomy [14]. The fixation of the contralateral ovary remains controversial. Some authors believe that this procedure should only be performed in recurrent torsion, elongated ovarian ligaments, and bilateral torsion of “normal” appendages when the cause of torsion has not been established [8, 14, 34, 37, 39].

DISCUSSION

Uterine lateroflexion is often overlooked in contemporary Russian and foreign literature. The literature mainly describes the transient deviation of the organ toward torsion, associating it with the “mass effect”, which is suppressed after detorsion. The term “mass effect” is widely used and has transitioned from adult to pediatric gynecology. The uterus deviates toward a torsioned ovary, which is often associated with a large mass of a cystically altered or tumor-containing appendage [20, 21]. However, interpreting the condition becomes difficult when the uterus is displaced toward the torsion of the “unchanged” appendage or to the contralateral side. Theoretically, this situation can be explained by reversing the cause-and-effect relationship, i.e., lateroflexion causes torsion.

In summary, three disease phases can be conditionally distinguished: predictor phase, acute phase (torsion), and recovery phase (up to 3 years after detorsion), each of which requires a detailed study. The first two phases will be considered because the recovery phase is exclusive to the gynecology section.

Some surgical aspects that require discussion based on objective evidence are as follows:

1. Predictor phase and simultaneous surgeries: Confirmative laparoscopy is generally recognized as necessary in severe abdominal pain syndrome and when acute surgical pathology cannot be excluded. The presence of ovarian cystic formations on preoperative ultrasound does not affect diagnostic techniques. If surgical pathology is ruled out, the next step is to determine the appropriate course of action for the cyst. Most cases are simple functional cysts that do not require intervention, particularly if the gonad is not larger than 4 cm. If the ovary measures >5 cm, the risk of torsion and malignant cell dissemination in patients without oncomarker testing must be considered. In our experience, we tend to avoid puncture. The situation is different when parovarian and paratubar cysts are detected. Because of their benign nature, growth, and refractoriness to conservative treatment, enucleation is necessary regardless of the mass size. In Morgagni cysts, removal is only recommended for attachments larger than 1 cm in diameter and on a long pedicle. All girls with cystic and tumorous uterine appendage masses detected during diagnostic procedures must be referred to a gynecologist.
2. Acute phase (torsion): The extent of surgical intervention required is dependent on the severity of ischemic disorders in the ovary and fallopian tube. Thus, the aim is to preserve even black appendages, as long as they remain intact. Tissues that disintegrate during detorsion must be removed. In the presence of cystic masses that caused AT, a detorsion is performed, without damaging the capsule. If the mass wall has ruptured, the ovary is resected within the healthy tissue. These procedures are considered necessary because of the high probability of bleeding. The greatest blood loss volume was 1,700 mL. The approach to ovarian fixation is individualized. During the acute phase, ipsilateral medial plication of the broad ligament with suturing to the round ligament of the uterus is preferred because of its anatomical advantages. The fixation of the ovary to the lateral pelvic wall is not recommended because it is considered unnecessary and traumatic during this period. However, in some cases, fixation is completely rejected because of severe ischemic disorders, the child is <8 years old (if the appendages have not descended into the pelvis, ovariopexy in an interval order is recommended), causes of torsion have been eliminated (such as enucleation of cysts, resection of a cystic ovary, or removal of parovarian masses), or a combination of these factors. Bilateral fixation is performed if intraoperative uterine lateroflexion is established, and both ovaries are located atypically.

CONCLUSIONS

The following AT predictors were identified based on an analysis of literature data and our experience: paramesonephric masses of uterine appendages, ovarian enlargement of >5 cm regardless of etiology, and uterine lateroflexion with atypical location of the ovary and fallopian tube.

With regard to treatment techniques for girls with AT, the following recommendations are followed in the clinic:

• If ovarian cysts are detected without torsion, transfer the patient to the gynecological department or consult a gynecologist.
• Enucleation of the mass is necessary to detect a paramesonephric cyst.
• Surgery on the ovary during the acute phase after uterine appendage detorsion is not recommended because of the risk of bleeding.
• If the appendage is twisted and the mass is disrupted, remove the cyst or resect the ovary while preserving healthy tissue and consult a gynecologist.
• Medial plication is the preferred method of oophoropexy.
• Bilateral oophoropexy is indicated after detorsion when the atypical location of the ovary and fallopian tube is caused by uterine lateroflexion

ADDITIONAL INFORMATION

Authors’ contribution. All authors made a substantial contribution to the conception of the work, acquisition analysis, interpretation of data for the work, drafting and revising the work, final approval of the version to be published and agree to be accountable for all aspects of the work. Personal contributions of each author: D.V. Donskoy — surgical treatment of patients, literature review, collection and analysis of literary sources, writing; A.V. Vilesov — surgical treatment of patients, patient supervision, collection and analysis of literary sources, article editing; R.A. Akhmatov, S.A. Korovin — surgical treatment of patients, collection and analysis of literary sources, article editing; K.D. Sangare — patient supervision, collection and analysis of literary sources, article editing; O.A. Alimova — patient supervision, collection and analysis of literary sources.

Funding source. This study was not supported by any external sources of funding.

Competing interests. Authors declare that they have no competing interests.

Consent for publication. Written consent was obtained from the patients for publication of relevant medical information and all of accompanying images within the manuscript.

ДОПОЛНИТЕЛЬНАЯ ИНФОРМАЦИЯ

Вклад авторов. Все авторы внесли существенный вклад в разработку концепции, проведение исследования и подготовку статьи, прочли и одобрили финальную версию перед публикацией. Вклад каждого автора: Д.В. Донской — хирургическое лечение пациентов, обзор литературы, сбор и анализ литературных источников, написание текста; А.В. Вилесов — хирургическое лечение пациентов, курация пациентов, сбор и анализ литературных источников, редактирование статьи; Р.А. Ахматов, С.А. Коровин — хирургическое лечение пациентов, сбор и анализ литературных источников, редактирование статьи; К.Д. Сангаре — курация пациентов, сбор и анализ литературных источников; О.А. Алимова — хирургическое лечение пациентов, сбор и анализ литературных источников.

Источник финансирования. Авторы заявляют об отсутствии внешнего финансирования при проведении исследования и подготовке публикации.

Конфликт интересов. Авторы декларируют отсутствие явных и потенциальных конфликтов интересов, связанных с публикацией настоящей статьи

Информированное согласие на публикацию. Авторы получили письменное согласие законных представителей пациентов на публикацию медицинских данных и фотографий.

About the authors

Dmitry V. Donskoy

Russian Medical Academy of Continuous Professional Education; Children’s State Hospital of St. Vladimir

Author for correspondence.
Email: dvdonskoy@gmail.com
ORCID iD: 0000-0001-5076-2378
SPIN-code: 8584-8933

MD, Cand. Sci. (Medicine)

Россия, Moscow; Moscow

Sergey A. Korovin

Russian Medical Academy of Continuous Professional Education

Email: korovinsa@mail.ru
ORCID iD: 0000-0002-8030-9926
SPIN-code: 2091-6381

MD, Dr. Sci. (Medicine)

Россия, Moscow

Alexey V. Vilesov

Children’s State Hospital of St. Vladimir

Email: vilesov.alexej@yandex.ru
ORCID iD: 0009-0001-4545-9590
SPIN-code: 2081-3871
Россия, Moscow

Roman А. Akhmatov

Russian Medical Academy of Continuous Professional Education; Children’s State Hospital of St. Vladimir

Email: Romaahmatov@yandex.ru
ORCID iD: 0000-0002-5415-0499
SPIN-code: 9024-8324
Россия, Moscow; Moscow

Kadidiatou D. Sangare

Russian Medical Academy of Continuous Professional Education

Email: tanti_sangare@yahoo.fr
ORCID iD: 0000-0003-2395-5777
Россия, Moscow

Olga A. Alimova

Children’s State Hospital of St. Vladimir

Email: dr.olga_andreevna@mail.ru
ORCID iD: 0009-0007-0679-885X
Россия, Moscow

References

Supplementary files