American Journal of Emergency Medicine 65 (2023) 43-52

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American Journal of Emergency Medicine

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Adnexal torsion in pregnancy: A systematic review of case reports and case series

Hamidreza Didar ^a, Hanieh Najafiarab ^a, Amirreza Keyvanfar ^b, Bahareh Hajikhani ^c,

Elena Ghotbi ^d, Seyyedeh Neda Kazemi ^e,f,?

^a Preventative Gynecology Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

^b Infectious Diseases and Tropical Medicine Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

^c Department of Microbiology, Shahid Beheshti University of Medical Sciences, Tehran, Iran

^d Department of Obstetrics and Gynecology, School of Medicine, Imam Hossein Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran

^e Clinical Research Development Center, Imam Hossein Educational Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran

^f Department of Obstetrics and Gynecology and Female Infertility Unit, Tehran University of Medical Sciences, Tehran, Iran

a r t i c l e i n f o

Article history:

Received 8 November 2022

Received in revised form 16 December 2022 Accepted 18 December 2022

Keywords: Adnexal diseases Ovarian torsion Ovariectomy Pregnancy

a b s t r a c t

Objectives: This study aimed to investigate clinical presentations, surgical procedures and findings, complications, and Predisposing factors of adnexal torsion in pregnant women.

Methods: We searched PubMed/Medline, Embase, and Web of Science from January 2000 to March 2022. All case reports and case series with full-text English language reporting adnexal torsion in pregnant women were in- cluded. Medical history, clinical presentations, surgical procedures and findings, complications related to adnexal torsion, and predisposing factors were independently extracted by two investigators.

Results: A total of 182 articles reporting 662 pregnant women with adnexal torsion were included. Most of the adnexal torsions occurred during the first trimester (54.63%), while others occurred during the second (26.36%) and third (19.00%) trimesters. The most common symptom of adnexal torsion was sudden-onset pain (80.60%). Enlargement of the adnexa was the most prevalent ultrasound finding in a twisted adnexa (95.20%). Additionally, about half of the patients had decreased blood flow in Doppler ultrasound (53.80%). Laparoscopic surgery was the favorite option (56.88%), while cystectomy and detorsion were the most commonly performed procedure (29.06%). Expectant management was reported in only 2.99% of the patients. In addition, the most common complications were preterm labor (27.58%) and emergent cesarean sections (25.28%). Conclusions: Clinicians should think of adnexal torsion when pregnant women complain of sudden-onset pain. Then, using ultrasound, adnexal enlargement or masses should be explored seriously. They should take invasive and ur- gent therapy to preserve ovaries and prevent complications.

(C) 2022

1. Introduction

Adnexal torsion is an uncommon but emergent condition in preg- nancy [1-3], which manifested with nonspecific symptoms. So, it can be misdiagnosed with other acute abdominal conditions such as appendicitis, renal colic, cholecystitis, intestinal obstruction, pelvic in- flammatory disease, ectopic pregnancy, ruptured ovarian cysts, and non-functional ovarian cysts [4].

Pregnancy is a risk factor for adnexal torsion as well as corpus luteum cyst, ovarian hyperstimulation syndrome (OHSS), and Assisted reproductive technologies (ART) [5]. Considering physiological and

* Corresponding author at: Clinical Research Development Center, Imam Hossein Educational Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

E-mail address: [email protected] (S.N. Kazemi).

anatomical alterations during pregnancy, it is challenging for clinicians to diagnose adnexal torsion in pregnant women. Early diagnosis and prompt operation are required to preserve adnexa. Moreover, abortion can be prevented by reducing ovarian edema or tissue necrosis and avoiding abdomen-pelvic inflammatory reactions [6,7]. The diagnosis of maternal adnexal torsion may be delayed in the second half of gesta- tion because of increased dimensions of the uterus, which causes diffi- culties in abdominal palpation and ultrasound [8]. Factors such as bloating, limited field of view (FOV), obesity, and anatomical alterations in late pregnancy can hinder the proper visualization of adnexal regions, making exploration of adnexal torsion complex [9]. Besides, to avoid the exposure of the fetus to radiation and iodinated contrasts, the computed tomography scan (CT-scan) is used in a limited way in pregnant women. So, most pregnant women suspected of adnexal torsion under- went an ultrasound [2].

https://doi.org/10.1016/j.ajem.2022.12.026

0735-6757/(C) 2022

If adnexal torsion is left untreated in pregnant women, it may lead to maternal morbidity, future infertility, and Fetal complications [1]. In early pregnancy, oophorectomy for removing the ovary containing the corpus luteum may lead to miscarriage. Hence, clinicians should con- sider expectant management when facing adnexal torsion, especially in young women with early pregnancy [10]. However, expectant man- agement through detorsion develops the risk of ovarian torsion recur- rence, which requires long-term follow-up [11].

This study was performed to answer the following questions: “What are the most common presenting symptoms and ultrasound findings of adnexal torsion in pregnancy?”; “What surgical approaches are typically utilized for adnexal torsion in pregnancy?”; “What intraoperative pa- thologies are commonly found in case of adnexal torsion in preg- nancy?”; “What are the most common predisposing factors of adnexal torsion in pregnancy?”

1. Methods

In this study, we followed the “Preferred Reporting Items for Sys- tematic Reviews and Meta-Analyses” (PRISMA) statement [12].

• 1. Literature search and study selection

We searched PubMed/Medline, Embase, and Web of science to iden- tify relevant studies published from January 2000 to March 2022. We used this query as the search strategy: (((Adnexal torsion) OR (tubo-ovarian torsion)) OR (ovarian torsion)) AND (pregnancy). Two reviewers independently screened the publications. We included case reports and case series with full-text English language reporting

adnexal torsion in pregnant women. We did not include published con- ference and professional society practical guidelines. Duplicate publica- tions, articles with no relevant data, and reviews or meta-analyses were excluded.

• 1. Data extraction

Two reviewers extracted the following data from the full texts of eligible publications: the first author’s name, date of publication, country, the total number of women with torsion, the total number of pregnant women with torsion, medical history, clinical presenta- tions (symptoms, signs, laboratory results and ultrasound findings), surgical procedures and findings (type of surgery, type of torsion, intra-operative visualization, and histopathology), complications re- lated to adnexal torsion, and predisposing factors. During the Review process, the reviewers resolved disagreements with a third individ- ual from the research team.

1. Results
   1. Study selection

The literature search revealed 1507 records initially. After re- moving duplicate publications, the titles and abstracts of 942 papers were screened. After applying the exclusion criteria to the full-text documents, 182 articles (142 case reports and 40 case series) with a total number of 662 pregnant patients with adnexal torsion met the inclusion criteria (Fig. 1). Table 1 presents the characteristics of included studies.

Fig. 1. Flow chart of study selection for inclusion in the systematic review.

Table 1

Characteristics of case reports/ case series.

References	Country	Published time	No. of women with ovarian torsion	No. of pregnant women with ovarian torsion	Age of pregnant women with ovarian torsion
Houry et al. [23]	USA	2000	87	12	NA
Chew et al. [24]	Singapore	2001	1	1	38
Abu-Musa et al. [25]	Lebanon	2001	1	1	26
Pinto et al. [26]	USA	2001	1	1	39
Phupong et al. [27]	Thailand	2001	1	1	34
Yaman et al. [28]	Austria	2002	1	1	32
Romer et al. [29]	Germany	2002	1	1	26
Gorkemli et al. [30]	Belgium	2002	9	6	32
Buser et al. [31]	USA	2002	1	1	22
Haenggi et al. [32]	Switzerland	2003	1	1	30
Huang et al. [33]	Taiwan	2003	1	1	35
Phupong et al. [34]	Thailand	2003	1	1	25
Romano et al. [35]	Israel	2003	1	1	27
Mathevet et al. [36]	France	2003	5	5	NA
Born et al. [37]	Germany	2004	1	1	22
Djavadian et al. [38]	Germany	2004	2	2	29
Pan et al. [39]	Taiwan	2004	1	1	35
Baksu et al. [40]	Turkey	2004	1	1	26
Vijayaraghavan et al. [41]	India	2004	21	1	NA
Roman et al. [42]	France	2005	1	1	26
Kumari et al. [43]	India	2005	5	5	NA
WU et al. [44]	Taiwan	2005	1	1	19
Oto et al. [45]	USA	2005	3	3	23.3
Djakovic et al. [46]	Germany	2006	1	1	26
Birchard et al. [47]	USA	2006	1	1	30
Rackow et al. [48]	USA	2007	2	2	28
Cornfeld et al. [49]	USA	2007	2	2	28.5
Upadhyay et al. [50]	USA	2007	2	2	33.9
Palanivelu et al. [51]	India	2007	1	1	30
Zanforlin Filho et al. [52]	Brazil	2008	1	1	29
Grgic et al. [53]	Croatia	2008	1	1	34
Renjit et al. [54]	Oman	2008	1	1	26
Rauf et al. [55]	UK	2008	1	1	22
Weitzman et al. [56]	USA	2008	2	2	32
DiLuigi et al. [57]	USA	2008	1	1	23
Silja et al. [58]	Oman	2008	1	1	32
Singh et al. [59]	India	2008	1	1	28
Wasik et al. [60]	UK	2008	1	1	29
Hasiakos et al. [4]	Greece	2008	4	4	30.25
Prefumo et al. [61]	Italy	2009	1	1	31
Christopoulos et al. [62]	Greece	2009	1	1	35
Varghese et al. [63]	Oman	2009	1	1	26
Arena et al. [64]	Italy	2009	1	1	38
Pezzuto et al. [65]	Italy	2009	1	1	33
Kolluru et al. [66]	India	2009	1	1	23
Eftekhar et al. [67]	Iran	2009	1	1	30
Oto et al. [2]	USA	2009	3	3	NA
Katz et al. [68]	Israel	2009	3	3	NA
Giulini et al. [69]	Italy	2010	1	1	31
Boswell et al. [70]	USA	2010	1	1	33
Ramesh et al. [71]	India	2010	1	1	29
Kayabasoglu et al. [72]	Turkey	2010	1	1	38
Efthimiadis et al. [73]	Greece	2010	1	1	NA
Chang et al. [74]	South Korea	2010	8	8	31.5
Terzic et al. [75]	Serbia	2011	1	1	31
Ten Cate et al. [76]	Belgium	2011	1	1	33
Simsek et al. [77]	Turkey	2011	1	1	27
Choudhary et al. [78]	India	2011	1	1	38
Shirokane et al. [79]	Japan	2011	1	1	37
Chohan et al. [80]	USA	2011	1	1	33
Al Omari et al. [81]	UAE	2011	2	2	30
Kibbey et al. [82]	Australia	2011	1	1	28
Uchil et al. [83]	UK	2011	1	1	21
Ergenoglu et al. [84]	Turkey	2011	1	1	30
Koo et al. [85]	South Korea	2011	55	55	30.8
Akl et al. [86]	USA	2012	1	1	32
Spitzer et al. [87]	Austria	2012	5	5	32.8
Ali et al. [3]	Egypt	2012	1	1	23
Passarinho et al. [88]	Portugal	2012	1	1	32
Shakir F [89]	UK	2012	1	1	37
Duncan et al. [90]	Australia	2012	1	1	28
Tsai et al. [91]	Taiwan	2012	1	1	32
Gaspar-Oishi et al. [92]	USA	2012	1	1	30
					(continued on next page)

References	Country	Published time	No. of women with ovarian torsion	No. of pregnant women with ovarian torsion	Age of pregnant women with ovarian torsion
Behar et al. [93]	Brazil	2012	1	1	20
Tsafrir et al. [94]	Israel	2012	216	48	NA
Lazaridis et al. [95]	UK	2013	1	1	39
Kaido et al. [96]	Japan	2013	1	1	30
Tsai et al. [97]	Taiwan	2013	3	3	33
Morton et al. [98]	USA	2013	1	1	30
Dursun et al. [99]	Turkey	2013	1	1	NA
Munshi et al. [100]	India	2013	1	1	26
Frederick et al. [101]	Jamaica	2013	1	1	32
Maurice et al. [102]	USA	2013	1	1	28
Perez-Rodriguez et al. [103]	Puerto Rico	2013	1	1	27
Sidiropoulou et al. [104]	Portugal	2014	1	1	36
Chandrasekar et al. [105]	UK	2014	1	1	33
Buke et al. [106]	Turkey	2014	1	1	26
El-Agwany et al. [107]	Egypt	2014	1	1	26
Bakacak et al. [108]	Turkey	2014	1	1	18
Yildirim et al. [109]	Turkey	2014	1	1	25
Sun et al. [110]	China	2014	1	1	32
Aydin et al. [111]	Turkey	2014	1	1	28
Tan et al. [112]	Taiwan	2014	1	1	28
Al-Badawi et al. [113]	Saudi Arabia	2014	2	2	34.5
Feng et al. [114]	China	2014	1	1	26
Priyadharisini et al. [115]	India	2014	1	1	22
Abdullah Agha et al. [116]	UK	2014	1	1	23
Graziano et al. [117]	Italy	2014	1	1	28
Kaur et al. [118]	UK	2014	1	1	28
Surampudi et al. [119]	India	2014	18	18	NA
Takeda et al. [120]	Japan	2014	3	3	NA
Ekin et al. [121]	Turkey	2015	1	1	26
Kim et al. [122]	South Korea	2015	1	1	29
Polat et al. [123]	Turkey	2015	1	1	36
Mathew et al. [124]	Oman	2015	1	1	22
Lee et al. [125]	South Korea	2015	1	1	35
Rouzi et al. [126]	Saudi Arabia	2015	1	1	29
Li et al. [127]	China	2015	1	1	27
Smolinski et al. [128]	USA	2015	1	1	28
Ozler et al. [129]	Turkey	2015	1	1	18
Williams et al. [130]	UK	2015	1	1	36
Iyswaria et al. [131]	India	2015	1	1	25
Kim et al. [132]	Korea	2015	1	1	35
Basaranoglu et al. [133]	Turkey	2015	132	24	29
Habek et al. [134]	Croatia	2016	1	1	32
Petresin et al. [135]	Germany	2016	1	1	33
Lai et al. [136]	China	2016	1	1	26
Kahramanoglu et al. [137]	Turkey	2016	1	1	32
Ozlu et al. [138]	Turkey	2016	1	1	25
Wyckoff et al. [139]	USA	2016	1	1	20
Ding et al. [140]	Taiwan	2016	1	1	17
Kim et al. [141]	South Korea	2016	1	1	35
Warda et al. [142]	USA	2016	1	1	37
Gobara et al. [143]	Japan	2016	1	1	24
Koumoutsea et al. [144]	UK	2016	1	1	33
Ramirez et al. [145]	USA	2016	1	1	27
Ganesh et al. [146]	India	2016	1	1	23
Guraslan et al. [147]	Turkey	2016	1	1	30
Karatas et al. [148]	Turkey	2016	1	1	27
Vaswani et al. [149]	India	2016	1	1	31
Minig et al. [150]	Spain	2016	4	4	30.75
Bras et al. [151]	Portugal	2017	1	1	27
Kaur et al. [152]	India	2017	1	1	24
Prabhu et al. [153]	India	2017	1	1	19
Young et al. [1]	USA	2017	1	1	34
Bouquet et al. [154]	Switzerland	2017	1	1	27
Navarro et al. [155]	Spain	2017	1	1	30
Kunovsky et al. [156]	Czech Republic	2017	1	1	35
Nasiri et al. [157]	USA	2017	1	1	31
Guterman et al. [158]	France	2017	4	4	35.5
Asch et al. [159]	USA	2017	6	6	NA
Hosny et al. [160]	Egypt	2017	7	4	NA
Ferrari et al. [7]	Italy	2018	1	1	34
Shore et al. [161]	Canada	2018	1	1	37
Jones et al. [162]	UK	2018	1	1	38
Al Salmi et al. [163]	Canada	2018	2	2	33.5
Li et al. [6]	China	2018	1	1	36
Soundararajan et al. [164]	India	2018	3	3	NA
Tankou et al. [165]	USA	2018	60	9	NA

References	Country	Published time	No. of women with ovarian torsion	No. of pregnant women with ovarian torsion	Age of pregnant women with ovarian torsion
Tanaka et al. [166]	Japan	2019	1	1	33
Levin et al. [167]	Israel	2019	1	1	28
Khalife et al. [168]	Lebanon	2019	1	1	31
Park et al. [169]	S. Korea	2019	1	1	36
Halimeh et al. [170]	Lebanon	2019	1	1	32
Kanayama et al. [11]	Japan	2019	1	1	40
Uyanikoglu et al. [171]	Turkey	2019	1	1	37
Hua et al. [172]	China	2019	1	1	25
Guennoun et al. [173]	Morocco	2019	3	3	22
Chavan et al. [174]	India	2019	7	7	NA
Yu et al. [175]	China	2019	5	5	NA
Butureanu et al. [176]	Romania	2019	6	6	NA
Wang et al. [22]	China	2019	174	143	NA
Sun et al. [177]	China	2019	17	17	28.5
Camelia et al. [178]	Romania	2020	3	3	NA
Yildirim et al. [179]	Turkey	2020	1	1	28
Bai et al. [9]	China	2020	1	1	27
Bacalbas,a et al. [180]	Romania	2020	1	1	27
Takeda et al. [181]	Japan	2020	1	1	30
Conte et al. [182]	Morocco	2020	2	2	28.5
Cagle-Colon et al. [183]	USA	2020	1	1	21
Hacioglu et al. [184]	Turkey	2020	1	1	40
Wang et al. [185]	China	2020	82	82	28
Rasekhjahromi et al. [186]	Iran	2020	1	1	28
Bernigaud et al. [187]	France	2021	1	1	34
Osto et al. [188]	USA	2021	1	1	22
Thomas et al. [189]	USA	2021	1	1	27
Ijarotimi et al. [190]	Nigeria	2021	1	1	29
Harou et al. [191]	Morocco	2021	1	1	40
Getaneh et al. [192]	USA	2021	1	1	28
Elbaum et al. [193]	USA	2021	1	1	26
Yu et al. [194]	China	2021	1	1	32
Lee et al. [195]	South Korea	2022	1	1	35

NA = not available.

• 1. Medical history of the patients

Most of the adnexal torsions in pregnancy occurred during the first trimester (230/421, 54.63%); others occurred during the second (111/ 421, 26.36%) and third (80/421, 19.00%) trimesters. Also, the data of the remaining 241patients were not reported. Regarding past obstetri- cal history, available data was limited: 10 cases had a previous natural vaginal delivery (10/101, 9.90%), 21 patients had a history of cesarean section (21/244, 8.60%), and the remainder of the studies reported no obstetrical history. Also, 28 women underwent abdominal surgeries other than cesarean section (28/103, 27.18%).

• 1. Clinical presentations of the patients

Table 2 shows the clinical presentations of the patients. The most com- mon location of pain was the right lower quadrant (RLQ) (97/194, 50.0%), followed by the left lower quadrant (LLQ) (42/194, 21.64%), hypogastric (36/194, 18.55%), and generalized pain (13/194, 6.70%). The most preva- lent quality of the pain was sudden onset (173/212, 81.60%), followed by constant (25/212, 11.79%), sharp (23/212, 10.84%), radiating (13/212, 6.70%), and colicky (1/212, 0.51%). On physical examination, the most common finding was local abdominal tenderness (127/195, 65.12%), followed by generalized abdominal tenderness (13/195, 6.66%).

Normal white blood cell (49/72, 68.05%) was more common than leukocytosis (23/72, 31.94%). Most cases had normal hemoglobin (32/ 42, 76.19%), while some had anemia (9/42, 21.42%).

The most common ultrasound findings were adnexal enlargement (101/106, 95.2%) and decreased blood flow (97/180, 53.8%). Also, 86 pa- tients reported simple ovarian cysts (86/116, 74.1%), and 46 reported complex ovarian cysts (46/102, 45.1%). Among studies indicating the size of the cyst, cysts ? 8 cm (32/56, 57.14%) were more prevalent than cysts >=8 cm (24/56, 42.85%).

• 1. Surgical procedures and findings

In this systematic review, adnexal torsion was approved in most cases (644/662) by surgical visualization, and the remaining cases (18/662) were diagnosed by ultrasound findings. Table 3 depicts surgical procedures and findings of the patients. In general, 163 studies mentioned how to treat pregnant women with adnexal torsion. Laparoscopic surgery (190/334, 56.88%) was more than open surgery (134/334, 40.11%) or expectant management (10/334, 2.99%). Additionally,

169 studies reported the exact procedures. The most common procedure was cystectomy and detorsion (100/344, 29.06%), followed by salpingo-oophorectomy (94/344, 27.32%) and solitary detorsion (63/344, 18.31%). Salpingectomy, oophorectomy, cystectomy, ovariopexy, and Combination therapy (e.g., detorsion and ligament plica- tion, cystectomy and ovariopexy, and others) were less common.

In studies reporting more detailed intra-operative findings, adnexal torsion was more prevalent on the right side (219/346, 63.29%) than on the left side (126/346, 36.41%) or bilateral (1/346, 0.28%). Overall, 214 patients had a net diagnosis of the type of torsion through surgery as follows: 77 adnexal torsions (including torsion of the ovary and fallopian tube) (35.98%), 73 isolated ovarian torsions (34.11%), 33 soli- tary cyst torsions (15.42%), and 28 isolated tubal torsions (13.08%).

Based on histopathology, the most common findings were corpus luteum (54/204, 26.47%), dermoid cyst (47/204, 23.03%), serous cyst adenoma (30/204, 14.70%), simple cyst (27/204, 13.23%), and hemor- rhagic or necrotic ovary (25/204, 12.25%).

• 1. Complications related to adnexal torsion

Forty-four studies reported at least one complication related to ad- nexal torsion. Among 87 complications, preterm labor (24/87, 27.58%) was on top of the list, followed by emergent cesarean section (C/S)

Table 2

Clinical presentations of the patients.

Variables Number of studies n/N* (%) Symptoms

Quality of pain

Table 3

Surgical procedures and findings.

Variables Number of studies n/N* (%) Type of surgery

Laparoscopic surgery 163 190/334 (56.88)

Sudden onset	98	173/212 (81.60)	Open surgery	163	134/334 (40.11)
Constant	98	25/212 (11.79)	Expectant management	163	10/334 (2.99)
Sharp	98	23/212 (10.84)	Cystectomy and detorsion	169	100/344 (29.06)
Radiating	98	16/212 (7.54)	Salpingo-oophorectomy	169	94/344 (27.32)
Colicky	98	12/212 (5.66)	Salitary detorsion	169	63/344 (18.31)
Location of pain			Salpingectomy	169	24/344 (6.97)
RLQ	141	97/194 (50.0)	Oophorectomy	169	24/344 (6.97)
LLQ	141	42/194 (21.64)	Cystectomy	169	21/344 (6.10)
Hypogastric	141	36/194(18.55)	Ovariopexy	169	11/344 (3.19)
Generalized	141	13/194 (6.70)	Combination therapy	169	7/344 (2.03)
RUQ or LUQ	141	1/194 (0.51)	Type of torsion
Other symptoms			Right side	159	219/346 (63.29)
Nausea	86	151/218 (69.26)	Left side	159	126/346 (36.41)
Vomiting	73	75/94 (79.78)	Bilateral	159	1/346 (0.28)
Fever	79	10/161 (6.21)	Adnexal torsion	156	77/214 (35.98)
Exam findings Local abdominal tenderness	109	127/195 (65.12)	Isolated ovarian torsion Solitary cyst torsion	156 159	73/214 (34.11) 33/214 (15.42)
Generalized Abdominal tenderness	109	13/195 (6.66)	Isolated tubal torsion	156	28/214 (13.08)
No tenderness	109	2/195 (1.02)	Pedunculated leiomyoma	156	2/214 (0.93)
Laboratory findings			Isolated infundibular torsion	156	1/214 (0.46)
Normal WBC	67	49/72 (68.05)	Intra-operative visualization & histopathology
Leukocytosis	67	23/72 (31.94)	Corpus luteum 93		54/204 (26.47)
Anemia	42	9/42 (21.42)	Dermoid cyst 93		47/204 (23.03)
Normal hemoglobin	42	32/42 (76.19)	Serous cyst adenoma 93		30/204 (14.70)
Elevated hemoglobin	42	1/72 (1.38)	Simple cyst 93		27/204 (13.23)
Elevated CRP	25	19/29 (65.51)	Hemorrhagic or necrotic ovary 93		25/204 (12.25)
Ultrasound findings			Malignant mass 93		6/204 (2.94)
Adnexal enlargement	62	101/106 (95.2)	Ectopic pregnancy 93		5/204 (2.45)
Decreased blood flow	74	97/180 (53.8)	Mucinous adenoma 93		4/204 (1.96)
Simple ovarian cyst	28	86/116 (74.1)	Endometriosis 93		4/204 (1.96)
Complex ovarian cyst	19	46/102 (45.1)	Ovarian leiomyoma 93		2/204 (0.98)

n, the number of patients with any variables; N, the total number of procedures OHSS: Ovarian hyperstimulation syndrome.

n, the number of patients with each variable; N, the total number of studied patients; EP, Ectopic pregnancy; LLQ, Left lower quadrant; LUQ, left upper quadrant; OHSS, Ovarian hy- perstimulation syndrome; RLQ, Right lower quadrant; RUQ, right upper quadrant; WBC, White blood cell.

Cysts <8 cm	48	32/56 (57.14)
Cyst >=8 cm	48	24/56 (42.85)
Ovarian superficiality	6	6/22 (27.27)
Ovarian edema	10	10/11 (91.0)
OHSS	14	15/16 (93.75)
EP	3	3/3 (100)
Increased vascularity in the ovary	2	2/2 (100)
Paratubal Cyst	4	4/5 (80.0)
Normal	6	6/6 (100)

Table 4

Complications related to adnexal torsion.

Variables Number of studies n/N (%)

Preterm labor 44 24/87 (27.58)

Emergent C/S 44 22/87 (25.28)

Miscarriage/abortion 44 14/87 (16.09)

Fetal/newborn complications 44 7/87 (8.04)

Leukocytosis is defined as WBC >= 13.6 x 10³/L for the first trimester, >= 14.8 x 10³/L for the second trimester, and >= 16.9 x 10³/L for the third trimester. Normal hemoglobin is defined as hemoglobin 11.6-13.9 mg/dL for the first trimester, 9.7-14.8 mg/dL for the second tri- mester, and 9.5-15.0 mg/dL for the third trimester [196].

Recurrence Preeclampsia

Others?

44 6/87 (6.89)

44 6/87 (6.89)

44 8/87 (9.19)

(22/87, 25.28%) and miscarriage/abortion (14/87, 16.09%). Other com- plications were reported in a few cases (Table 4).

• 1. Predisposing factors for adnexal torsion

Finally, we showed predisposing factors for adnexal torsion in Table 5. The most common predisposing factor for adnexal torsion was follicular/luteal cysts (133/495, 26.86%), followed by ART (132/ 495, 26.66%), ovarian complex cyst -dermoid cyst, serous cyst adenoma, and mucinous cyst adenoma- (98/495, 19.79%), OHSS (36/495, 7.27%), and paratubal cyst (28/495, 5.65%). Interestingly, few patients had no predisposing factor (19/495, 3.83%).

1. Discussion

Adnexal torsion is the fifth gynecologic emergency. Despite its rarity in pregnancy, the difficulties in diagnosis, treatment, and complications make it a tough challenge for clinicians [5].

Patients almost describe a sudden onset of sharp pain in addition to nausea and vomiting. On physical examination, the most common sign

n, the number of patients with each variable; N, the total number of patients with compli-

cations; C/S, cesarean-section.

* internal bleeding/hemoperitoneum (due to the cyst rupture), small bowel obstruc- tion, ileus, premature rupture of membrane (PROM), and hydronephrosis.

Table 5

Predisposing factors for adnexal torsion.

Variables	Number of studies	n/N* (%)
Follicular/Luteal cysts	169	133/495(26.86)
ART	169	132/495 (26.66)
Complex ovarian cyst	169	98/495 (19.79)
OHSS	169	36/495 (7.27)
Paratubal cyst	169	28/495 (5.65)
PCOS	169	15/495 (3.03)
Ovarian neoplasm	169	8/495 (1.61)
Ectopic pregnancy	169	7/495 (1.41)
Large ovary	169	6/495 (1.21)
Endometriosis	169	5/495 (1.01)
Elongation of adnexa	169	4/495 (0.80)
Hydrosalpinx/hematosalpinx	169	4/495 (0.80)

n, the number of patients with each variable; N, the total number of predisposing factors; OHSS, Ovarian hyperstimulation syndrome; PCOS, Polycystic ovarian syndrome.

is local tenderness. However, a few patients are febrile. These findings indicate an ischemic process due to a partial or complete rotation of ad- nexa. Since the process is acute, considerable changes in routine labora- tory tests are uncommon. In contrast, the CRP level was elevated in our study, which is generally higher in pregnant women than in non- pregnants [13].

Ultrasound is an applicable device for investigating the adnexa. Because of a gravid uterus and anatomical alterations in pregnancy, it has no maximum efficacy [14]. Definite diagnosis of adnexal is made by surgical visualization [15]. However, it is recommended to perform Ultrasound imaging due to the harmlessness and helpfulness. In a preg- nant woman with adnexal torsion, the most common finding in ultrasound is adnexal enlargement with or without a viable mass. Ac- cording to the literature, 80% of adnexal torsions are associated with masses >5 cm [14]. Our findings revealed a little increased chance of torsion in cysts larger than 8 cm. Although a normal ultrasound is rare in the case of torsion, it cannot rule out adnexal torsion [14]. Also, decreased blood flow of the ovarian artery using the Color Doppler method should consider an alarm for adnexal torsion. However, normal color Doppler findings will not rule it out [16].

Appendicitis is on top of the differential diagnoses of adnexal tor- sion. Appendicitis generally manifested with RLQ pain (the most com- mon site of pain in our study) and local tenderness, accompanied by nausea and vomiting. Due to the similar clinical manifestations and im- aging limitations in pregnant women mentioned above, adnexal torsion can be misdiagnosed with appendicitis. However, the mechanism of pain in torsion is ischemia, while the infection is the leading cause of ap- pendicitis [17]. In our study, about one-third of the patients had leuko- cytosis. Leukocytosis strongly predictors appendicitis, chorioamnionitis, and other infectious pregnancy complications. But, physicians should remember that adnexal torsion may also present with leukocytosis. Additionally, the presence of fever can help clinicians to distinguish between adnexal torsion and infection. Adnexal torsion is rarely accom- panied by fever [17], as most of our cases were afebrile.

Consistent with the literature, about two-thirds of the adnexal tor- sion occurs on the right side [18]. Because the right utero-ovarian liga- ment is longer than the left and the left sigmoid colon physically limits left ovary movement, the torsion on the right side is more com- mon. Most torsion events happen in the first trimester of pregnancy, probably by the impact of predisposing factors such as ART and Cysts (follicular or luteal cysts). However, the third trimester has the lowest incidents, probably due to the enlargement uterine, followed by the lim- itation of adnexa space for torsion. Also, during the third trimester, there is no luteal cyst nor ART effect to cause the adnexal torsion [18].

The most common finding on the histopathology was a functional cyst, including follicular and luteal cysts. It is explainable by the cyst for- mation during the stimulation of ovaries by ART [19]. Our study’s sec- ond pathology finding was dermoid cysts, contributing to 23% of all torsions in pregnant women. Dermoid cysts are the most common masses associated with torsion in non-pregnant women [20].

A population-based cohort study compared the surgical techniques and outcomes of 1366 pregnant women with torsion with non- pregnant women with torsion. The most predominant treatment was open surgery (57%), followed by expectant management (17%). The study mentioned that the laparoscopic technique (15%) was less com- mon than in previous studies [21]. However, in our review, laparoscopy had a higher rate with 56.88%, followed by laparotomy (40.11%). Expec- tant management only accounted for 2.99%. At first glance, an open sur- gery rate of 40.11% may seem very high for this condition. In this systematic study, case reports from the year 2000 to now have been considered. The rate of laparotomy may be skewed by time since lapa- roscopic surgery was less common in the past. Besides, some cases pre- sented initially with acute abdomen. It was unavoidable to perform laparotomy in these cases. In a retrospective study conducted in China, a higher proportion of non-pregnant women with torsion under- went expectant management than pregnant women with torsion (5%

vs. 19%). So, it can be hypothesized that adnexal torsion in pregnancy requires more invasive and urgent therapies [22]. Most procedures in our studies were cystectomy and detorsion (29.06%), followed by salpingo-oophorectomy (27.32%). However, in a previous study, salpingo-oophorectomy amounted to 52% of all procedures. This differ- ence can be attributed to the developments in surgical procedures and scientific advances. Traditionally, thromboembolism after detorsion of the adnexa and the higher recurrence rate encouraged surgeons to re- move the adnexa [21]. However, we report no thromboembolic event, and only 6 cases relapsed.

We may assume that some relevant articles are unintentionally ex- cluded despite searching multiple databases with proper queries. Also, we included published articles written in English, so there is a possible issue of language bias. Also, we only included case series and case re- ports. Other types of studies, published conferences, and professional society practical guidelines were not involved in our review.

1. Conclusions

When pregnant women present with sudden-onset pain (mainly on the RLQ), local tenderness, nausea, and vomiting, clinicians should think of adnexal torsion, especially in the lack of fever. Then, using ultrasound, adnexal enlargement or masses should be explored seriously. They should take invasive and urgent therapy to preserve ovaries and pre- vent complications.

Funding

This study received no financial support.

CRediT authorship contribution statement

Hamidreza Didar: Data curation, Conceptualization, Writing - original draft. Hanieh Najafiarab: Data curation, Writing - review & editing. Amirreza Keyvanfar: Writing - review & editing, Methodology, Formal analysis. Bahareh Hajikhani: Methodology, Formal analysis. Elena Ghotbi: Investigation, Data curation. Seyyedeh Neda Kazemi: Supervision, Writing - review & editing.

Declaration of Competing Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

We thank the Preventative Gynecology Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran, for their excellent collaboration.

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