Clinical efficacy of ultrasound-guided interventional therapy in patients with benign ovarian cysts: a meta-analysis

Abstract

This study aimed to explore the clinical efficacy of ultrasound-guided interventional therapy in patients with benign ovarian cysts through meta-analysis. A literature search was performed on PubMed, Web of Science, Embase, CNKI, and WanFang databases to obtain clinical randomized controlled trials on ultrasound-guided interventional therapy for benign ovarian cysts published between 2010 and 2022. A total of 1395 studies were initially retrieved, and finally 12 studies were included for meta-analysis. The results showed that the observation group (ultrasound-guided interventional therapy) had higher treatment effective rate than the control group (conventional laparotomy or laparoscopic cyst resection), but the incidence of adverse reactions was markedly lower. Additionally, the length of hospital stay, intraoperative blood loss, and operation time showed significant lower levels in the observation group. In terms of ovarian function, postoperative luteinizing hormone and follicle-stimulating hormone levels in the observation group were lower than the control group, while oestradiol levels were higher. In conclusion, compared with conventional surgical treatment, ultrasound-guided interventional therapy can significantly improve the clinical effective rate, shorten the hospital stay and reduce intraoperative blood loss. Such therapy can protect ovarian reserve, with high value of clinical promotion.

IMPACT STATEMENT

• What is already known on this subject? Main surgical methods for ovarian cysts consist of laparotomy, laparoscopic surgery, and interventional therapy.

• What the results of this study add? With the advancement of surgical techniques and instruments, many minimally invasive surgeries have been applied to treat ovarian cysts with good clinical results. However, there is no exact evidence to prove its clinical efficacy. Given the lack in this field, we conducted a meta-analysis of all clinical studies of ultrasound-guided interventional therapy for ovarian cysts to evaluate its efficacy and safety.

• What the implications are of these findings for clinical practice and/or further research? Compared with conventional laparotomic or laparoscopic cyst resection, ultrasound-guided interventional therapy for ovarian cysts significantly improves the treatment effectiveness, shortens the hospital stay and reduces intraoperative blood loss. This therapy with good clinical efficacy also has advantages of small wound, rapid recovery and less adverse reactions, and can protect ovarian reserve. This safe and effective surgical method for ovarian cysts is worth promoting clinically.

Keywords:

• Ultrasound
• interventional therapy
• benign ovarian cysts
• meta-analysis

Introduction

Ovarian cysts are a common benign gynaecological condition that is common in women of all ages. Most of these lesions are benign (Hizkiyahu et al. 2020). The prevalence in premenopausal and postmenopausal women is 35% and 17%, respectively (Pavlik et al. 2013). Some studies have shown that benign ovarian cysts may resolve spontaneously when they are <5 cm in diameter, but surgery may be an option for cysts >5 cm in diameter or larger and complex cysts (American College of Obstetricians and Gynecologists’ Committee on Practice Bulletins-Gynecology 2016). If left untreated, the cyst may rupture due to torsion of the tip, resulting in an acute abdomen (Wang et al. 2012). Currently, laparoscopic surgery is the gold standard for the treatment of benign ovarian cysts (Kostrzewa et al. 2019). And several studies (Eltabbakh et al. 2008) have confirmed the feasibility and safety of laparoscopic surgery for the treatment of large (≥10 cm) and benign ovarian cysts in women. Laparoscopy of benign ovarian cysts has been established as an alternative to open surgery; however, it also involves anaesthesia and hospitalization, and has some limitations, including ovarian cyst rupture, tumour overflow, incomplete tumour resection, trocar site metastasis, and direct cancer cell implantation (Tanaka et al. 2008).

Studies have shown that ultrasound-guided interventions are mostly used for gynaecological diseases, such as uterine fibroids and adenomyosis (Zhang et al. 2015). Ultrasound-guided percutaneous or transvaginal aspiration of benign ovarian cysts can be an alternative to surgical intervention, especially in high-risk surgical candidates (Fisch and Sher 2004, Duke et al. 2006). A clinical study (Zerem et al. 2009) found that in patients with benign ovarian cysts who were not suitable for open or laparoscopic surgery, none of the patients developed malignancy during follow-up after short-term ultrasound-guided percutaneous drainage with no serious complications. Nikolaou et al. (2014) used transvaginal ultrasound-guided ovarian cyst aspiration for benign ovarian cysts. They found no complications or excessive pelvic pain during or after the procedure in any of their patients. Although ultrasound-guided interventional treatment of ovarian cysts has been gradually promoted clinically in recent years because of its advantages, there is a lack of definite evidence of its clinical efficacy. Therefore, in this study, we performed a meta-analysis of all clinical studies of patients treated with ultrasound-guided interventions for benign ovarian cysts to systematically evaluate the effectiveness and safety of ultrasound-guided interventions.

Materials and methods

Search strategy

The protocol for this meta-analysis has been registered in the PROSPERO database and the registration number is 383481. This study followed the instruction of Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines. PubMed, Web of Science and Embase, China National Knowledge Infrastructure (CNKI), and WanFang databases were searched with the time span from 2010 to 2022. The following were valid terms and related variants used in database searches: ‘ultrasound’ AND ‘benign ovarian cyst’ OR ‘ovarian cyst’, AND ‘interventional therapy’ OR ‘interventional treatment’. The Chinese database was searched using the Chinese search terms listed above.

Inclusion and exclusion criteria

Inclusion criteria included: (1) Study design: Randomized controlled trials (RCTs) on ultrasound-guided interventional therapy for benign ovarian cysts that have been published in relevant medical journals at home and abroad; (2) Participants: Patients diagnosed with benign ovarian cyst by doctors; aged 18–50 years; ovarian cyst diameter ≤10 cm; with stable vital signs and good general condition; with surgical indications; (3) Intervention measures: The patients were divided into an observation group treated with transabdominal or transvaginal ultrasound-guided interventional therapy for benign ovarian cysts and a control group treated with conventional laparotomy or laparoscopic cyst resection; (4) Outcome measures: At least including one of the following indicators: ① clinical efficacy indicators: treatment effective rate (markedly effective: the cyst with a diameter <3 cm or completely disappearing; effective: the cyst with a diameter reduced to 1/2 of the original; ineffective: the size of the cyst is basically unchanged within 6 months of follow-up), incidence of adverse reactions; ② postoperative recovery indicators: hospital stay, intraoperative blood loss, operation time; ③ ovarian function indicators: oestradiol (E2), lutenizing hormone (LH), follicle stimulating hormone (FSH) and other ovarian function indicators.

Exclusion criteria were: ① Non-RCTs, or intervention measures inconsistent with the requirements of this meta-analysis; ② The original literature failed to provide the relevant data required for this meta-analysis; ③ Duplicate literature; ④ Literature with unclear diagnostic criteria or outcome measures.

Literature screening and data extraction

Duplicate literature was removed, and two reviewers independently screened the remaining articles in strict accordance with the inclusion and exclusion criteria, extracted data from eligible ones and evaluated their quality. Disagreements were solved by discussion with a third party to reach a consensus. Relevant data extracted included: (1) article title, author’s name, publication date, sample size, age; (2) study type; (3) surgical intervention measures; (4) clinical treatment effective rate, adverse reactions, operation time, blood loss, length of hospital stay, ovarian function indicators. Review Manager 5.30 software was used to assess the risk of bias according to the Cochrane Handbook for Systematic Evaluation of Interventions.

Statistical analysis

Data were statistically analysed using Stata 16.0 statistical software. Odds ratio (OR) and its 95% confidence interval (CI) were used to express enumeration data, and standardized mean difference (SMD) and 95% CI to express continuous variables. Heterogeneity across studies was assessed using the chi-square test. P > 0.10 and I² ≤ 50% indicated no statistical heterogeneity, and the fixed-effects models were used; otherwise a random-effects model was selected. P < 0.05 was considered statistically significant.

Results

Basic information of included studies

In this study, a total of 1395 articles were obtained from the initial search. Then 189 duplicate records were excluded, and 1194 studies that did not meet the inclusion criteria were removed. Finally, 12 RCTs were included (Li 2020, Hu 2016, Dong 2018, Huang and Wang 2018, Jiao et al. 2018, Teng and Li 2018, Zhong 2018, He et al. 2020, Jiang 2020, Lv 2020, Gong 2022). The literature screening process is shown in Figure 1. A total of 1098 patients with benign ovarian cysts were included in the study, with 554 patients in the observation group and 544 patients in the control group. The included subjects were women of reproductive age (aged 19.78-48.95), with disease course ranging from 0.88 to 17.59 years. The characteristics of the included studies are displayed in Table 1. The risk of bias graph and risk of bias summary are shown in Supplementary Figure S1(A,B).

Figure 1. Flow chart of literature screening.

Table 1. The basic characteristics of included literature.

Study	Year	Sample time	Group	Cases	Age (years)	Course of disease	Study design	Outcome measures
Jiang Fusheng	2020	2016/11-2018/09	Treat	50	33.42 ± 3.82	NP	RCT	①③④⑤
			Cont	50	35.23±4.32	NP
Zhong Shujuan	2018	2014/05-2018/05	Treat	29	35.0±4.1	9.5±1.5	RCT	②③④⑥
			Cont	29	37.5±4.3	8.0±1.3
Teng Fengqin	2018	2016/01-2017/12	Treat	105	28.6±3.4	8.4±2.1	RCT	①③⑤
			Cont	95	28.8±3.2	8.3±2.2
Li Xiaofei	2013	2011/10-2012/01	Treat	58	26±2.8	NP	RCT	①②③④
			Cont	58	26±2.8	NP
Hu Qing	2016	2015/02-2016/02	Treat	27	28.58±8.80	NP	RCT	①②③④
			Cont	27	29.01±8.56	NP
Dong Jinbo	2018	2017/01-2017/12	Treat	65	26.38±2.44	1.34±0.27	RCT	①⑥
			Cont	65	26.72±2.15	1.21±0.33
Jiao Ruishuang	2018	2016/07-2017/08	Treat	24	27.13±3.91	1.33±0.78	RCT	①⑥
			Cont	24	26.92±4.21	1.28±0.73
Lv Hongmei	2020	2019/01-2019/10	Treat	60	36.4±2.1	2.6±0.5	RCT	①②
			Cont	60	36.4±5.1	2.7±0.4
Li Dandan	2020	2016/01-2018/10	Treat	25	32.5±2.2	9.3±1.8	RCT	③④⑤
			Cont	25	32.4±2.2	9.4±1.9
Huang Rui	2018	2017/08-2018/07	Treat	24	40.13±1.10	2.09±0.36	RCT	①⑥
			Cont	24	40.12±1.11	2.06±0.39
He Jinliang	2020	2018/08-2019/08	Treat	46	36.64±12.31	13.42±4.17	RCT	①②③④
			Cont	46	35.78±11.86	12.54±4.32
Gong Aihua	2022	2020/01-2020/12	Treat	41	40.28±6.11	2.09±0.94	RCT	①②③④⑤
			Cont	41	40.19±6.24	2.14±0.89

Obse: Observation; Con: Control; M: Male; NP: Not reported; RCT: Randomized controlled trial; ①Effective rate after treatment; ②Incidence of adverse reactions; ③Postoperative hospital stay; ④Intraoperative blood loss; ⑤Time of operation; ⑥Postoperative oestradiol levels; Postoperative luteinizing hormone levels; Postoperative follicle stimulating hormone levels.

Meta-analysis results of effective rate and incidence rate of adverse reactions after treatment

Among the RCTs included in this meta-analysis, a total of 10 (Li 2013, Hu 2016, Dong 2018, Huang and Wang 2018, Jiao et al. 2018, Teng and Li 2018, He et al. 2020, Jiang 2020, Lv 2020, Gong 2022) studies compared the treatment effective rate between two treatment methods for benign ovarian cysts, and 6 (Li 2013, Hu 2016, Zhong 2018, He et al. 2020, Lv 2020, Gong 2022) studies compared the incidence of adverse reactions between the two groups. There was no significant heterogeneity among the studies (treatment effective rate: I² = 0.0%, P = 0.858; incidence of adverse reactions: I² = 0.0%, P = 0.596). Ultrasound-guided interventional therapy for benign ovarian cysts produced a significantly higher effective rate and lower incidence of adverse reactions than that of conventional laparotomy or laparoscopic cyst resection [effective rate: OR = 5.15, 95% CI (3.08, 8.61), P < 0.001; Figure 2(A); incidence of adverse reactions: OR = 0.26, 95% CI (0.16, 0.43), P < 0.001; Figure 2(B)]. Further sensitivity analysis was performed for these two indicators to test the robustness of the study results. After individual studies were excluded one by one, the estimate and 95% CI did not change significantly, indicating high robustness of the analysis results (Figure 3(A,B)).

Figure 2. Forest plots comparing the clinical efficacy in two groups of patients with benign ovarian cysts (A: effective rate; B: incidence of adverse reactions).

Figure 3. Sensitivity analysis of clinical efficacy in two groups of patients with benign ovarian cysts (A: effective rate; B: incidence of adverse reactions).

Meta-analysis results of postoperative recovery indicators

Eight studies (Li 2013, 2020, Hu 2016, Teng and Li 2018, Zhong 2018, He et al. 2020, Jiang 2020, Gong 2022) compared the length of hospital stay between the two groups, 7 (Li 2013, 2020, Hu 2016, Zhong 2018, He et al. 2020, Jiang 2020, Gong 2022) reported their intraoperative blood loss, and 4 (Teng and Li 2018, Jiang 2020, Li 2020, Gong 2022) compared operation time. There was significant heterogeneity among the studies (hospital stay: I² = 94.7%, P < 0.001; intraoperative blood loss: I² = 97.3%, P < 0.001; operation time: I² = 97.7%, P < 0.001), so the random-effects model was used for statistical analysis. The observation group had significant shorter hospital stay [SMD = −2.341, 95% CI (−3.160, −1.523), P < 0.001; Supplementary Figure S2(A)], intraoperative blood loss [SMD = −2.697, 95% CI (−4.096, −1.297), P < 0.001; Supplementary Figure S2(B)], and operation time [SMD = −3.340, 95% CI (−5.233, −1.448), P = 0.001; Supplementary Figure S2(C)] compared with the control group.

Further sensitivity analyses were performed to test the robustness of the results of the postoperative recovery measures. There was no significant difference in the estimated value and 95% CI when studies regarding hospital stay, postoperative blood loss or operation time were excluded one by one, respectively. Such results suggested the results of this study were robust (Supplementary Figure S3(A–C)).

Meta-analysis results of ovarian function indicators

Five RCTs (Dong 2018, Huang and Wang 2018, Jiao et al. 2018, Zhong 2018, Lv 2020) compared postoperative E2 levels in two groups, four (Dong 2018, Huang and Wang 2018, Jiao et al. 2018, Zhong 2018) compared LH levels, and 7 (Dong 2018, Huang and Wang 2018, Jiao et al. 2018, Zhong 2018, Jiang 2020, Li 2020, Lv 2020) compared FSH levels. The random-effects model was used for statistical analysis (E2 level: I² = 89.7%, P < 0.001; LH level: I² = 93.3%, P < 0.001; FSH level: I² = 97.2%, P < 0.001). Compared with the control group, E2 levels [SMD = 1.181, 95% CI (0.256, 2.106), P = 0.012; Supplementary Figure S4(A)] after ultrasound-guided interventional treatment were significantly higher, while LH [SMD = −1.260, 95% CI (−2.427, −0.092), P = 0.034; Supplementary Figure S4(B)] and FSH [SMD = −2.159, 95% CI (−4.240, −0.078), P = 0.042; Supplementary Figure S4(C)] showed lower levels.

For determination of the robustness of the results. Sensitivity analysis was carried out by removing each study one by one; after that, the estimated value and 95% CI of postoperative E2 level, LH level and FSH level were not significantly different from the original results. Thus, it could be considered that the robustness of the results of this study was good (Supplementary Figure S5(A–C)).

Discussion

In recent years, with the continuous development of medical techniques and minimally invasive techniques, laparoscopic surgery has gradually become the first choice for benign ovarian cysts because of its minimal wound, rapid recovery, and ability to meet the aesthetic requirements of patients (Han and Feng 2013, Falcetta et al. 2016). However, some studies have concluded that laparoscopic surgery can affect the ovarian reserve function of patients (Li et al. 2009, Sweed et al. 2019). Therefore, ultrasound-guided interventional therapy has been rapidly applied clinically due to its small wound, rapid recovery, and no effect on ovarian reserve. In this study, we systematically evaluated the effectiveness and safety of ultrasound-guided interventions in the clinical management of patients with benign ovarian cysts. After a comprehensive literature search and evaluation, 12 studies were finally included for meta-analysis. The results suggest that, compared with laparotomy or laparoscopic surgical treatment, ultrasound-guided intervention significantly improves the treatment efficiency, shortens the hospital stay, and reduces intraoperative bleeding in patients with benign ovarian cysts, while helping to preserve ovarian reserve function. This indicates that the technique can be widely promoted for clinical treatment.

Clinically, the treatment effective rate and the incidence of adverse reactions are commonly used to evaluate the effectiveness and safety of surgery. This study found that the effective rate of ultrasound-guided interventional therapy for benign ovarian cysts was significantly higher than that of conventional laparotomy or laparoscopic cyst resection, while the observation group had a lower incidence of adverse reactions. In the study by Li (2020), the efficiency of ultrasound interventional treatment was significantly higher than conventional open cystectomy, and the incidence of complications (e.g. sweating, fever, flushing) was significantly lower. This may be due to the traditional laparotomy with its large incisions, slow wound recovery, postoperative infections and complications. In contrast, ultrasound-guided interventional therapy allows for a good surgical field of view, clear observation of subtle lesions, facilitates complete removal of the lesion, and has a lower risk of recurrence (Gao et al. 2009).

Further, we found that the hospital stay and intraoperative bleeding were significantly less in the observation group than in the control group, indicating that the surgery and recovery were better in ultrasound-guided interventional therapy. This is consistent with the results of the study by Li et al. (2012), in which the intraoperative bleeding and operative time of ultrasound-guided interventional surgery for ovarian cysts were less than those of traditional open surgery. The reason for better postoperative recovery of the observation group may be that ultrasound-guided interventional therapy can achieve fully exposure of cyst lesions under the surgical field, but not pulling the greater omentum as well as the intestinal canals. Such therapy therefore causes positive effects on surgical operation, blood loss, postoperative recovery, and length of postoperative hospital stay (Duan and Sun 2016).

Ovarian function is a critical indicator for assessing female sex hormone secretion and ovulation ability, and reduced ovarian function can affect female fertility (Iwase et al. 2010). At present, LH, FSH, E2 and other sex hormones are commonly used to assess ovarian reserve in clinical practice (Laven and Fauser 2006). In the present meta-analysis, E2 levels were significantly higher in patients after ultrasound intervention than in the control group, while LH and FSH levels were significantly lower. Previous studies have reported that surgical treatment of benign ovarian cysts results in damage to follicles and granulosa cells in the ovary, which affects the level of benign ovarian cysts (Ergun et al. 2015). The reason why ultrasound-guided interventional therapy has less impact on the body is that it causes less damage to ovarian follicles and granulosa cells than conventional surgery (Xu et al. 2019).

This meta-analysis has the following limitations. First, although an extensive literature search was conducted, the 12 included studies were all in Chinese and the small sample size of each study would affect the final results, resulting in insufficient statistical efficacy. Second, the follow-up time of some studies was unclear, and long-term follow-up was required for this analysis. Third, the literature included for each observation was small, and subgroup analysis and funnel plot assessment of publication bias could not be performed. Therefore, future multicentre clinical studies are needed to confirm the findings.

Conclusions

In summary, compared with conventional laparotomy or laparoscopic cyst resection, ultrasound-guided interventional therapy for benign ovarian cysts significantly improves the treatment effectiveness, shortens the hospital stay and reduces intraoperative blood loss. This therapy with good clinical efficacy also has advantages of small wound, rapid recovery and less adverse reactions, and can protect ovarian reserve. This safe and effective surgical method for benign ovarian cysts is worth promoting clinically.

Ethics approval and consent to participate

This is a meta-analysis and ethics approval and consent to participate are not required.

Consent for publication

Not applicable.

Author contributions

The data for the validation was gathered by Zuoxi He. Statistical analyses were performed by Yukun Lu and Zuoxi He. The manuscript was chiefly written by Yuedong He. The study was designed by Yukun Lu and Yuedong He. All authors review the manuscript.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability statement

The datasets analysed during the current study are available from the corresponding author on reasonable request

Additional information

Funding

The author(s) reported there is no funding associated with the work featured in this article.