Results
Their demographic and clinical characteristics are described in Table 1 . There were no significant differences between the two groups in terms of age, number of pregnancies, size of cysts, history of pelvic surgery or assisted reproductive techniques. The gestational age at onset differed between the two groups: in the laparoscopy group, 83.3% of women were in the first trimester, 16.7% were in the second trimester, while in the laparotomy group, 22.6% of women were in the first trimester, 35.8% were in the second trimester and 41.5% were in the third trimester.
Table 1 Clinic characteristics of the two groups Characteristics Laparoscopy( N = 102) Laparotomy( N = 53) Statistic P value Age (years) 27.89 ± 4.70 26.62 ± 3.42 T = 1.919 0.057 Gravidity (times) 1.0(1.0–2.0) 1.0(1.0–2.0) Ζ = 0.523 0.128 Parity (times) 0.0(0.0–1.0) 0.0(0.0–0.0) Ζ=-1.043 0.161 History of pelvic surgery ( n , %) 23(22.5%) 7(13.2%) χ2 = 1.950 0.163 IVF ( n , %) 14(13.7%) 3(5.6%) χ2 = 2.323 0.127 OHSS ( n , %) 10(9.8%) 1(1.9%) χ2 = 2.224 0.136 Mass size (cm) 7.5(6.0–9.0) 7.0(5.0–9.0) Ζ=-1.722 0.085 Emergency surgery ( n , %) 90(88.2%) 48(90.6%) χ2 = 0.194 0.660 Twins rate ( n , %) 5(4.9%) 1(1.9%) χ2 = 0.215 0.643 Gestational age at onset First trimester ( n , %) 85(83.3%) 12(22.6%) χ2 = 68.394 0.000 Second trimester ( n , %) 17(16.7%) 19(35.8%) Third trimester ( n , %) 0 22(41.5%) Results presented as mean ± SD, frequency (percentage) or median (interquartile range) IVF : assisted reproductive technique OHSS : ovarian hyperstimulation syndrome
Clinic characteristics of the two groups
Results presented as mean ± SD, frequency (percentage) or median (interquartile range)
IVF : assisted reproductive technique
OHSS : ovarian hyperstimulation syndrome
The operative characteristics of the patients in the study cohort are presented in Table 2 . There was no difference in the number of adnexal twists between the two groups. Most torsion cases were managed by removal of the involved adnexal cyst. If ovarian necrosis was severe, the affected adnexa should be removed concurrently. There was no significant difference between the two groups in terms of surgical type, including salpingo-oophorectomy, oophorectomy and cystectomy. However, the amount of blood loss, length of hospital stay and incidence of delayed-healing wounds in the laparotomy group were significantly greater than those in the laparoscopy group ( P < .05). Elsewhere, the median gestational age at surgery was 10.1 weeks (range: 8.1–13.0) in the laparoscopy group and 24.4 weeks (range: 14.4–38.0) in the laparotomy group.
Table 2 Surgical details of the two groups Surgical details Laparoscopy( N = 102) Laparotomy( N = 53) Statistic P value Number of adnexal twists (times) 2.0(1.0-2.5) 2.0(1.5–2.75) Ζ-0.601 0.548 Gestational age at surgery (weeks) 10.1(8.1–13.0) 24.4(14.4–29.5) Ζ-7.577 0.000 Operation time (minutes) 61.5(44.7–82.0) 63.0(46.0–80.0) Ζ-0.447 0.655 blood loss (ml) 17.5(10.0–30.0) 20.0(20.0–50.0) Ζ-2.895 0.004 delayed-healing wounds ( n , %) 1(1.0%) 6(11.3%) χ2 = 6.416 0.011 hospital stay (days) 5.0(4.0–6.0) 8.0(6.0–12.0) χ2=-7.071 0.000 Type of surgery Cystectomy ( n , %) 54(52.9%) 26(49.1%) χ2 = 0.211 0.646 Unilateral salpingo-oophorectomy ( n , %) 41(40.2%) 23(43.4%) χ2 = 0.186 0.666 Unilateral salpingectomy ( n , %) 2(2.0%) 4(7.5%) χ2 = 1.616 0.204 Detorsion alone ( n , %) 4(3.9%) 0 χ2 = 0.300 0.184 Aspiration ( n , %) 1(1.0%) 0 χ2 = 1.000 0.658 Results presented as frequency (percentage) or median (interquartile range)
Surgical details of the two groups
Results presented as frequency (percentage) or median (interquartile range)
The pathological characteristics are shown in Table 3 . The main pathological types were luteal cysts in the laparoscopy group and mature teratomas in the laparotomy group. In the laparoscopy group, detorsion alone was performed in three patients, and cyst aspiration was performed in one patient with a history of OHSS. In 18 patients, tissue ischemia and necrosis were badly damaged, and the pathological types could not be distinguished. All the pathological findings were benign except for 1 patient with borderline mucinous cystadenoma. The most common histopathological diagnosis was benign cystic teratoma (47.8%, 22/46); the second most common histopathological diagnosis was mesosalpinx cyst (17.4%, 8/46) in the laparotomy group; the most common histopathological diagnosis was corpus luteum cyst (48.9%, 43/88); and the second most common histopathological diagnosis was benign cystic teratoma (15.9%, 14/88) in the laparoscopy group.
Table 3 Pathologic diagnoses (%) of the two groups Histology Laparoscopy( N = 88) Laparotomy( N = 46) Mature cystic teratoma ( n , %) 14(15.9%) 22(47.8%) Corpus luteum ( n , %) 43(48.9%) 6(13.0%) Paraovarian cyst ( n , %) 10(11.4%) 2(4.3%) Paratubal cyst ( n , %) 6(6.8%) 8(17.4%) Endometriosis ( n , %) 1(1.1%) 2(4.3%) Follicular cyst ( n , %) 2(2.2%) 0 Serous cystadenoma ( n , %) 5(5.7%) 3(6.5%) Mucinous cystadenoma ( n , %) 6(6.8%) 3(6.5%) Borderline mucinous tumor ( n , %) 1(1.1%) 0 Results presented as frequency (percentage)
Pathologic diagnoses (%) of the two groups
Results presented as frequency (percentage)
Obstetric outcomes were evaluated in 101 women in the laparoscopy group and 51 women in the laparotomy group (Table 4 ). Progesterone therapy or inhibition of uterine contractions was routinely given to patients before 34 weeks after surgery, and uterine contractions were no longer inhibited after 34 weeks. Ultrasound was routinely performed before discharge to determine the presence of fetal heartbeats. All patients recovered well after surgery, without thrombosis, massive bleeding, or sepsis. Among these patients, two (2.3%) in the laparoscopy group and two (3.8%) in the laparotomy group were lost to follow-up after surgery. Artificial abortion was performed in one patient in the laparotomy group and 13 patients in the laparoscopy group because of an unplanned pregnancy. There were no significant differences between the two groups in terms of the rate of miscarriages, mode of pregnancy termination, gestational delivery, birth weight, neonatal intensive care unit, or rate of preterm delivery. A total of 7 miscarriages occurred in the laparoscopic group, 6 of which occurred within the first postoperative week. A total of 2 abortion in the laparotomy group, one was occurred within the first week after surgery.
Table 4 Obstetric outcome of the two groups Obstetric outcome Laparoscopy( N = 102) Laparotomy( N = 53) Statistic P value Miscarriage rate ( n , %) 7(8.0%) 2(3.8%) χ2 = 0.615 0.433 Preterm birth (< 37 weeks) ( n , %) 8(10.1%) 5(10.4%) χ2 = 0.003 0.958 Caesarean delivery ( n , %) 53(67.1%) 29(60.4%) χ2 = 0.581 0.446 delivery gestations (weeks) 39.0(38.0-39.3) 39.0(38.0-39.3) Ζ=-0.399 0.690 Birth weight (g) 3275(2985–3600) 3350(2870–3600) Ζ=-1.709 0.087 NICU admission 11(13.1%) 9(18.4%) χ2 = 0.673 0.412 Artificial abortion ( n , %) 14(12.7%) 1(1.9%) / / Loss to follow-up 2(2.3%) 2(3.8%) / / Results presented as frequency (percentage) or median (interquartile range) NICU: Neonatal Intensive Care Unit
Obstetric outcome of the two groups
Results presented as frequency (percentage) or median (interquartile range)
NICU: Neonatal Intensive Care Unit
Conclusion
AT is a rare, frequently misdiagnosed condition during pregnancy that is associated with a high rate of morbidity. Once AT is suspected, laparoscopy is a minimally invasive diagnostic method. On the basis of our retrospective study, laparoscopy for treating AT during pregnancy may be more beneficial than laparotomy. Further prospective comparisons of pregnant women with confirmed AT during pregnancy are needed to validate our results.
Discussion
In the present study, we compared different surgical approaches for treating AT during pregnancy over a 10-year period in our hospital, and 155 patients were included. The present article was based on a large study comparing precise obstetric outcomes between laparotomy and laparoscopy. The results indicated that laparoscopic surgery for AT during pregnancy had better surgical outcomes, shorter lengths of hospital stay, less surgical bleeding and delayed-healing wounds than did laparotomy. No significant differences were observed between the groups in terms of fetal loss, preterm delivery, birth weight, delivery mode or neonatal intensive care unit admission.
The most common clinical symptom of torsion is intermittent, sudden-onset abdominal pain associated with nausea and vomiting. The diagnosis of AT is more challenging during pregnancy because these clinical symptoms are also typical for uterus rupture, placental abruption, urethral or renal colic, and hemolysis, elevated liver enzymes, low platelets (HELLP) syndrome. Transabdominal ultrasound is the preferred method for the examination of AT [ 7 ]. It forms the foundation of diagnostic evaluation due to its ability to directly and rapidly evaluate both ovarian anatomy and perfusion. In our study, ultrasound was first performed in all 155 (100%) patients, and the most common ultrasound finding was an enlarged adnexal cyst with an average diameter of more than 7 cm in both groups. Ultrasonography findings suggestive of ovarian torsion include unilateral ovarian enlargement and ovarian edema with a coiled vascular pedicle (referred to as the “whirlpool sign”). The “whirlpool sign”, which is the main hallmark seen on imaging, is usually observed [ 8 ]. Nevertheless, it was previously reported [ 9 ] that Doppler ultrasonography was normal in 60% of patients despite the presence of ovarian torsion, and a normal ultrasound examination cannot exclude this diagnosis. Djavadian et al. [ 10 ] demonstrated that in 15% of 38 patients, the initial diagnosis was incorrect from the time of hospitalization to surgery.
AT is a surgical diagnosis. Daykan et al. [ 11 ] reported that surgery during pregnancy for suspected AT was not a risk factor for preterm labor and did not lead to adverse pregnancy or neonatal outcomes. Considering maternal and fetal safety, surgery should be performed in a timely manner when the patient is diagnosed. Thus, the uterus is obviously enlarged during the middle and late periods, and the space available for surgery is limited. The evidence thus far suggests that laparoscopy can be performed during any trimester of pregnancy, including the third trimester [ 12 , 13 ]. In terms of the near-term effects, the first thing is to reduce the spontaneous abortion rate of surgical intervention. Wilasrusmee et al. [ 14 ] reported in a meta-analysis that the risk of spontaneous abortion and preterm delivery was significantly greater among pregnant women with suspected appendicitis in the laparoscopy group than among those who underwent laparotomy. Rottenstreich et al. [ 5 ] demonstrated that the use of a laparoscopic procedure during the early stages of pregnancy was associated with increased rates of miscarriage. However, many reports had discussed the relative safety of laparoscopy compared with that of laparotomy. Similar to previous studies [ 4 , 11 , 15 ], no significant difference in fetal loss or preterm labor was observed between the two groups in our study. Cagino et al. [ 16 ] concluded that laparoscopy did not increase the risk of spontaneous abortion or preterm delivery based on a systematic review and meta-analysis of large samples. However, unlike other results originating from adnexal masses, which have precluded comparisons between laparoscopy and laparotomy. Our study focused on the comparison of surgical methods in cases of AT, which was unique. Doğan et al. [ 17 ] reported a case of heterotopic pregnancy treated with transvaginal natural orifice transluminal endoscopic surgery (vNOTES), which was a less invasive alternative to laparoscopy. Perhaps someday vNOTES may be used in cases of AT during pregnancy.
The potential effects of CO2 insufflation on the fetus have also led to apprehension over its use. Because CO2 exchange occurs with intraperitoneal insufflation, there has been concern about the effects of acidosis [ 18 ]. Sun B et al. [ 19 ] reported that a CO2 pneumoperitoneum duration of less than one hour had no effect on the growth hormone (GH)–insulin-like growth factor I (IGF-I) axis, while a longer duration of CO2 pneumoperitoneum progressively inhibited the GH–IGF-I axis. This meant that maximizing surgical time could reduce the effects of CO2 pneumoperitoneum. If the torsion mass is malignant, it is not practical to complete laparoscopic surgery for a long time.
In addition, we found that the probability of delayed incision healing of more than seven days in the laparotomy group was significantly greater than that in the laparoscopy group. All six cases of delayed incision healing occurred in the third trimester of pregnancy, and two of them were sutured twice. Postoperative uterine contractions may repeatedly irritate the wound and affect its healing.
Regarding the long-term effects of surgery, Daykan et al. [ 11 ] demonstrated that there were no significant differences in birth weight, gestational duration, intrauterine growth restriction, infant death, or fetal malformation between patients who underwent laparoscopy and those who underwent laparotomy for singleton pregnancies. In our study, we compared delivery gestation, delivery mode, and newborn weight between the two groups, and there were no significant differences. This suggests that neither laparoscopy nor laparotomy affects long-term pregnancy outcomes.
The occurrence of cancer during pregnancy is an uncommon event, occurring in approximately 1.26 of 1000 pregnancies [ 20 ]. A meta-analysis revealed that the incidence of ovarian cancer in patients with AT was 1% [ 21 ]. When surgery is required for known or suspected malignancies, laparotomy is a better approach for optimal visualization to minimize postoperative uterine irritability and contractions [ 22 , 23 ]. The vast majority of AT tumors are benign, with only one borderline mucinous tumor in the laparoscopy group in this study. Conservative treatment includes only untwisting the adnexa and aspirating any associated cyst [ 24 ]. Thus, we conducted detorsion alone in three patients and cyst aspiration in one patient with a history of OHSS. Corpus luteum cysts were more common in the laparoscopy group than in the laparotomy group. Torsion of the corpus luteum cyst most commonly occurs during the first trimester because it usually disappears by 12 to 16 weeks.
Our study also had a few limitations. First, this was a retrospective study in one center, and bias due to incomplete data might have created this study. Second, the gestation weeks at surgery of the two groups were not at the same baseline level because surgeons were more inclined to choose laparotomy in middle-late pregnancy.
Introduction
Adnexal torsion occurs when the ovary and fallopian tube twist on the axis created between the infundibulopelvic ligament and the utero-ovarian ligament. It generally involves only the ovary and rarely involves only the fallopian tube. It can occur in patients of any age but is not commonly found in women during pregnancy. Pregnancy is a risk factor for AT, with an estimated incidence of 1–5:10,000 of all pregnancies [ 1 , 2 ].
Early diagnosis and prompt treatment of AT are critical for preserving ovarian tissue and preserving future function. However, the diagnosis of AT during pregnancy is often difficult due to its nonspecific signs and symptoms. Changes in the position of the ovaries and fallopian tubes with an enlarged uterus increase the difficulty of diagnosis. Misdiagnosis or delayed treatment can lead to ovarian necrosis, abortion, premature delivery and other risks. The clinical incidence of AT during pregnancy is low, and surgical treatment is mostly limited to small sample studies [ 3 , 4 ].
In addition, laparoscopy during pregnancy requires consideration of specific intraoperative surgical risks as well as the pregnancy’s obstetric outcomes. Rottenstreich et al. [ 5 ] demonstrated via logistic regression analysis that the performance of laparoscopy prior to 8 weeks of gestation was an independent factor associated with miscarriage. Pregnancy status and an enlarged uterus may affect treatment decisions. Due to the enlargement of the uterus, both traditional laparotomy and laparoscopic surgery are limited by the abdominal space. Bassi et al. [ 6 ] reported that only 16% of pregnant women underwent laparoscopy, and 9% of them underwent conversion to open surgery.
The present study aimed to compare the surgical and obstetric outcomes of laparotomy and laparoscopic surgery and to evaluate the efficacy of laparoscopic surgery for treating AT during pregnancy.
Materials|Methods
This was a retrospective cohort study in one medical center in China after approval by the institutional review board. The electronic medical records of patients who were hospitalized between July 2012 and July 2023 at The First Affiliated Hospital of Zhengzhou University were reviewed. Through retrospective case analysis, the keywords “torsion of ovary”, “adnexal torsion”, “pregnancy”, “torsion of ovarian cyst” and “torsion of fallopian tube” were used as search keywords. The number of pregnant women hospitalized during this period was 99,126, and a total of 159 pregnant women were diagnosed with AT by surgery, with an overall incidence of 0.16/100. Four patients who underwent cesarean section and adnexal cyst resection in late pregnancy were not included. The indications for surgery included sudden-onset abdominal pain and persistent masses on sonography. All laparoscopic surgeries were performed under general endotracheal anesthesia, whereas laparotomy was performed under regional anesthesia. The patients were divided into 2 groups according to the surgical method used: 53 patients were included in the traditional laparotomy group, and 102 patients were included in the laparoscopy group.
Clinical, ultrasound, surgical and pathological data were retrospectively retrieved from the medical records. The clinical information included the patient’s age, parity, mode of conception, gestational age, symptoms and signs, surgical data, postoperative pathology and pregnancy outcome. The operative time was calculated from the beginning to the end of anesthesia. We defined delayed-healing wounds as healing of the abdominal incision for more than seven days. Pregnancy outcome follow-up included the miscarriage rate, time of termination of pregnancy, method of termination of pregnancy, fetal weight, etc. Sonographic data were collected retrospectively from the last examination reports. The maximum diameter of the three sections was used as the reference data. The gestational trimesters were classified as follows: (1) first trimester, 12 weeks or before; (2) second trimester, 13–27 weeks; and (3) third trimester, 28 weeks and above.
Follow-up was conducted by medical records inquiry and telephone follow-up. The telephone questionnaire was administered by a physician using a standard script, which was uploaded to the supplement file . After providing verbal informed consent, the participants were asked about their pregnancy outcomes (live birth or abortion) and gestational age of delivery, etc.
The data analysis was carried out using SPSS 26.0 statistical analysis software (IBM Inc., Chicago, IL). Normally distributed continuous variables are reported as the mean ± standard deviation; nonnormally distributed variables are reported as the median and interquartile range. Categorical variables are reported as counts and proportions. Univariate analyses, including the chi-square test or Fisher’s exact test, were used to compare categorical variables. Continuous variables were tested by unpaired Student’s t tests or Mann‒Whitney tests, depending on the distribution of the continuous variables. Statistical significance was indicated at P < .05.
Supplementary Material
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