1. Introduction
The adhesion of the inner wall of the uterus , known as intrauterine adhesions (IUA), often leads to complete or partial occlusion of the uterine cavity and some subsequent clinical symptoms.[ 1–3 ] IUA cause occlusion of the uterine cavity because it can damage the endometrium.[ 2 , 4 ] Severe IUA affect embryo implantation and sperm migration, which cause lower pregnancy and live birth rates.[ 1 , 5 , 6 ] Transcervical resection of adhesion (TCRA), a standard surgical approach for patients with IUA, is widely used for treating moderate and severe IUA patients.[ 7–10 ] TCRA is performed under hysteroscopy to separate and remove scar tissues and restore the structure of uterine cavity and protect the remaining endometrium.[ 11 , 12 ] However, women with moderate to severe IUA have a high recurrence rate after TCRA, and their reproductive outcomes remain a concern.[ 7 ]
Currently, few studies investigate the reproductive outcomes of women with moderate and severe IUA after TCRA, and heterogeneity of these results is high.[ 13 ] First, it is thought that there are some confounders in the studies that may affect the reproductive outcome, including the severity of IUA, the medical situation of the participants, the length of follow up, and other potential factors.[ 14 , 15 ] Besides, the confidence intervals of study results are wide.[ 16 ] Therefore, a systematic review is necessary to be conducted to combine the results of various studies. The aim of this study was to review all existing literature to investigate reproductive outcomes after TCRA in women with moderate and severe IUA.
2. Methods
2.1. Search strategy
We conducted a scoping review by using 4 databases, including Google Scholar, PubMed, Scopus, Embase and web of science, to retrieve relevant literature from September 1, 2001 to February 1, 2023. This paper used following search terms: “Asherman syndrome” OR “intrauterine adhesion” AND (“severe intrauterine adhesion” OR “moderate intrauterine adhesion”) AND (“pregnancy” OR “pregnancy rate” OR “miscarriage” OR “reproductive outcomes” OR “pregnancy outcomes”) [Title/Abstract], “uterine adhesion” OR “uterine synechiae”) AND (“pregnancy” OR “pregnancy rate” OR “miscarriage” OR “reproductive outcomes” OR “pregnancy outcomes”) AND (“severe intrauterine adhesion” OR “moderate intrauterine adhesion”) [Title/Abstract].
2.2. Inclusion criteria
Randomized controlled trials (RCTs) or cohort studies that report reproductive outcomes after TCRA in women with moderate to severe IUA will be included.
Original articles published in peer-reviewed journals must be in the form of complete papers.
2.3. Exclusion criteria
Abstracts, repeated publications, and articles that did not contain expected results.
Articles that were not in English.
Studies, reviews, and animal studies that included fewer than 10 participants.
2.4. Quality assessment and systematic review
Literature screening, data extraction, and bias risk assessment were systematically performed by 2 independent reviewers. Two reviewers screened the papers according to the inclusion and exclusion criteria. Relevant data including first author, study design, study period, age, intervention measurement, pregnancy rate, methods of conception, and live birth rate were extracted using a form created specifically for this review. All data extraction was double-checked.
The Cochrane tool and the Newcastle-Ottawa scale was used to conduct quality assessment to assess potential bias by 2 reviewers.[ 17 , 18 ] The Cochrane risk of bias tool is divided into “low risk,” “unclear risk,” and “high risk” in 7 specific areas: random sequence generation, allocation concealment, selective reporting, other sources of bias, blinding (participants and personnel), blinding (outcome assessment), and incomplete outcome data.[ 17 ] The Newcastle-Ottawa scale was adapted to evaluate retrospective studies in 7 aspects: representativeness of the exposed cohort, selection of the nonexposed cohort, ascertainment of exposure, demonstration that the outcome of interest was not present at the start of the study, comparability of cohorts based on the design or analysis, assessment of outcome, follow-up long enough for outcomes to occur, and adequacy of follow up of cohorts.[ 18 ] Moreover, preferred reporting items for systematic reviews and meta-analyses flow was made according to the requirements of the systematic review to demonstrate the literature screening process.[ 19 ] The studies were approved by the ethics committee of Fuzhou Maternity and Infant Hospital.
2.5. Statistical analysis
Data analysis was achieved by RevMan 5.4.1 (The Cochrane Collaboration, London, United Kingdom), and heterogeneity was assessed using I 2 . Heterogeneity was considered small when I 2 was <25% and high when I 2 was >75%.[ 20 ] A 2-sided P value ≤ .05 is considered statistical significance.[ 21 ]
3. Results
3.1. Characteristics of the included studies
The procedures for screening and selecting of eligible studies were demonstrated by using the preferred reporting items for systematic reviews and meta-analyses flow chart[ 19 ] (Fig. 1 ). First, we identified 19 potential papers describing the reproductive results of women with moderate or severe IUA after TCRA. Nine articles were excluded because of incomplete data or improper study design. After excluding duplicates, 10 articles were retained. Among them, 3 were RCT studies (Fig. 2 ), 1 was a prospective study, and 6 were retrospective studies. This study has included a total of 2099 participants. Moreover, a description of the characteristics of the included studies is provided (Tables 1 and 2 ).
Table 1 -
Characteristics of the included studies.
Study
Design
No. of cases
Study period
Age of patients
Post-TCRA treatment
Pregnancy rate
Method of conception
Mean time from TCRA to pregnancy
Live birth rate
Huang XW 2020
RCT
171
Aug. 2016–Dec. 2017
31.69 ± 5.268
Balloon uterine stent/IUD plus a ley catheter
60.2%
41.9% naturally
13.4 ± 5.4 mo.
54.2%
Sun JH. 2020
Retro
156
Apr. 2017–Jan. 2019
34.16 ± 5.02
Intrauterine balloon
39.7%
43.8% naturally
-
-
Zhang XM 2021
RCT
96
Jan. 2016–Dec. 2019
29.8 ± 4.18
IUD/Foley1w + IUD/Foley1M + IUD;
46.9%
-
9.7 ± 3.7 mo
-
Chen LM 2017
Retro
357
Jan. 2012 and Dec. 2015
28.4 ± 6.1
Oestradiol valerate 4 mg/d for 7 d, 3 mg/d for 7 d, and estradiol valerate 2 mg/d, medroxyprogesterone acetate 10 mg/d for 7 d.
40.0%
-
9.7 ± 3.7 mo,
<85.6%
Zhu R 2019
Retro
236
Jan. 2013 and Mar. 2016
31.4 ± 4.8
Oestradiol valerate 4 mg/d for 21 d
40.9%
--
-
Roy KK 2009
Retro
89
Jan. 2002–Dec. 2006
28.4
Stent
32.6%
-
12.8 mo
77.8%
Chen YQ 2017
Pro
114
-
30.77 ± 4.40
IUD. estradiol valerate 3 mg/d thrice daily. medroxyprogesterone 10 mg/d for 3 cycles.
44.3%
Natural conception:28 patients IVF: 15 patients.
14.2 ± 5.6 mo
27.8%
Shi X 2019
RCT
191
15 May 2017 and 22 Nov. 2017
32.0 ± 4.4
IUB
28.7%
-
-
-
Chen Q 2016
Retro
332
Jan. 2012 and Dec. 2015
28.4 ± 6.1
Estradiol valerate 4 mg/d for 7 d, then 3 mg/d for 7 d, and then estradiol valerate 2 mg/d and medroxyprogesterone acetate 10 mg/d for 7 d.
-
-
-
-
Xu 2018
Retro
357
January 2010 to January 2016.
30.48 ± 4.16
Balloons were removed 1 week later and the IUD removed either 1 wk later or during a second-look hysteroscopic examination.
-
-
-
75%
IUA = intrauterine adhesions, IUB = intrauterine balloon, IUD = intrauterine devices, Pro = prospective cohort study, RCT = randomized controlled trial, Retro = retrospective study, TCRA = transcervical resection of adhesion.
Table 2 -
Newcastle-Ottawa quality assessment scale for cohort studies.
Study groups
Representativeness of the exposed cohort
Selection of the nonexposed cohort
Ascertainment of exposure
Demonstration outcome of interest not present at the start of the study
Comparability of cases and controls on the basis of design or analysis
Assessment of the outcome
Follow up for outcome to occur
Adequacy of follow up of cohorts
Chen L 2017
Yes
NI
NI
Yes
NI
Yes
Yes
Yes
Chen Y 2017
Yes
Yes
Yes
Yes
NI
Yes
Yes
Yes
Sun JH 2020
Yes
Yes
Yes
Yes
NI
Yes
Yes
Yes
Roy KK 2010
PN
NI
Yes
Yes
NI
Yes
Yes
Yes
Zhu R 2019
Yes
NI
Yes
Yes
NI
Yes
Yes
Yes
Chen Q 2016
Yes
Yes
Yes
NI
Yes
Yes
NI
NI
Xu W 2018
Yes
NI
Yes
Yes
NI
NI
NI
Yes
NI = no information, PN = Probably no.
Figure 1.: Prisma flow is illustrated. PRISMA = preferred reporting items for systematic reviews and meta-analyses.
Figure 2.: Cochrane bias tool for potential bias and quality assessment of RCT studies. RCT = randomized controlled trial.
3.2. Quality assessment and meta-analysis results
The quality assessment results were: 5 high-quality articles, 4 medium-quality articles, and 1 low-quality article (Table 1 ). In our study, we found that the pregnancy rate of participants was between 28.7% and 60.2%. The live birth rate was between 27.8% and 85.6%. The duration from TCRA surgery to pregnancy was 9.7 months to 14.2 months.
The risk difference of pregnancy rate of the included studies was 1.75 [1.17, 2.62], which was clinically significant but not statistically significant. The heterogeneity of the risk difference was low (I 2 = 19%) (Fig. 3 ). The risk difference of hypermenorrhoea and amenorrhea were −0.28 [−0.37, −0.19] and −0.06 [−0.26, 0.13], respectively, and the heterogeneity was low (I 2 = 0%) (Fig. 4 ). The risk difference of pregnancy rate in the 2 retrospectives studies was 2.26,[ 22 , 23 ] with a 95% confidence range of 1.99 to 2.58. The pooled term of live birth rate was 11.30 (95% CI: 9.39–13.59) (Fig. 5 ).
Figure 3.: Forest plot comparing the pregnancy rate after and before TCRA. TCRA = transcervical resection of adhesion.
Figure 4.: Forest plot comparing the menstrual status after and before TCRA. TCRA = transcervical resection of adhesion.
Figure 5.: Forest plot comparing the pregnancy rate and live birth rate in 2 retrospective studies.
4. Discussion
IUA seriously damages fertility function and causes infertility, especially in women with moderate to severe symptoms.[ 24 ] TCRA plays a crucial role in the treatment of women with moderate and severe IUA. TCRA can accurately observe the location of the lesion and separate adhesions under hysteroscopy.[ 25 ] However, women with moderate to severe IUA have a high recurrence rate of IUA, which increases concerns about their reproductive outcomes after TCRA.[ 7 ] Here, our study showed that the live birth rate and pregnancy rate of participants after TCRA were significantly higher than those of participants without TCRA. The pregnancy and live birth rates ranged from 28.7% to 60.3% and 27.8% to <85.6%, respectively. Moreover, the menstruation status significantly improved after TCRA.[ 22 , 26–29 ] The improvement rates ranged from 88.2% to 100%.
Evidence has revealed that the pregnancy and live birth rates of women after TCRA are significantly increasing, which may be due to the use of adjuvant treatments after surgery.[ 1 , 30 ] To date, surgeons often use estrogen to restore the underlying endometrium after TCRA.[ 2 , 31 , 32 ] Oestrogen is believed to promote the growth and regeneration of the endometrium.[ 33 ] The regenerated endometrium quickly covers the fibrotic scars of the previous adhesions, accelerates the epithelialisation of the exposed areas, and prevents readhesion.[ 34 ] However, there are no specific guidelines on the time and dose of administration.[ 35 ] Some studies recommend taking 2.5 mg of equine estrogen daily for 2 or 3 cycles.[ 36–38 ] This was also reflected in our included studies, and 6 included studies used estrogen to prevent readhesion after surgery.[ 39–42 ]
Other methods include the insertion of intrauterine devices (IUDs) and balloons.[ 43 ] It is believed that IUD and balloons can separate the anterior and posterior walls of the uterus through a physical barrier to prevent readhesion of the uterine cavity.[ 44 ] In an RCT study, IUD was found to be effective in preventing recurrence and improving productive outcomes.[ 35 ] Approximately 73% of women experienced a menstrual recovery, 31% became pregnant, and the live birth rate was 16%.[ 36 , 45 , 46 ] In addition, studies on the combined use of IUDs and other adjuvant treatments have reported pregnancy rates ranging from 8.9% to 99.9% and live birth rates ranging from 5.23% to 99.8%.[ 47 ] However, Charles et al pointed out that there are some concerns regarding the use of IUDs and balloons.[ 48 ] The copper-containing IUD and the descending tube of the balloon may cause excessive inflammation.[ 5 ] In addition, no study has investigated the specific type and duration of the effects of IUDs.[ 23 , 49 , 50 ]
The major disadvantage of this study is that it included many retrospective studies and did not allow us to access the relevant information. The included studies recorded and analyzed potential confounders that may affect IUA or reproductive outcomes, such as previous uterine surgery, age, gestational age at delivery or abortion, interval between delivery/abortion, and other interventions (such as inserting intrauterine balloon, intrauterine balloon). In addition, the included studies need to be involved a large number of participants.
5. Conclusion
TCRA is the standard surgery for the treatment of moderate to severe IUA.[ 51 ] It has effectively enhanced the reproductive outcomes of women with moderate to severe IUA.[ 30 ] In this study, we found that pregnancy and live birth rates were increased significantly after TCRA, and the menstrual status of women also was improved. Altogether, TCRA is the useful approach for the treatment of moderate to severe IUA for promoting the reproductive outcomes in women.
Acknowledgements
We thank our colleagues for their critical comments.
Author contributions
Conceptualization: Hong Jiang, Yong Xia.
Data curation: Meifang He, Qiuli Chen, Jinlian He, Qingqing Zhao.
Formal analysis: Meifang He, Qiuli Chen, Jinlian He, Qingqing Zhao.
Investigation: Qiuli Chen, Qingqing Zhao.
Methodology: Meifang He, Qiuli Chen, Jinlian He, Qingqing Zhao.
Project administration: Hong Jiang, Yong Xia.
Resources: Qiuli Chen, Jinlian He, Qingqing Zhao.
Software: Jinlian He, Qingqing Zhao.
Supervision: Hong Jiang, Yong Xia.
Validation: Hong Jiang, Yong Xia.
Visualization: Hong Jiang, Yong Xia.
Writing – original draft: Meifang He, Qiuli Chen.
Writing – review & editing: Hong Jiang, Yong Xia.
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