The Top 100 Most Cited Articles on Intrauterine Adhesion: A Bibliometric Analysis

Abstract

Background: Bibliometric analysis is a statistical method which attempts to assess articles by their citations, analyzing their frequency and pattern of citing phenomenon. Through the analysis, some guidance can be extracted for future research directions. Over the past few years, there have been articles published in mounting numbers focused on intrauterine adhesions. Nevertheless, little is known about the properties and qualities of these researches. No existed analysis commits to reflecting the progress of researches in intrauterine adhesion.

Methods: Web of Science Core Collection, BIOSIS Citation Index and MEDLINE were searched for the identifying articles released from 1950 to October 2020. Articles concerning about Intrauterine adhesion were determined. Subsequently, the 100 most cited articles were chosen for analysis of citation count, citation density (citations/article age), authorship, theme, geographic distribution, time-related flux, level of evidence, and network analysis.

Results: An overwhelming majority of the certain 100 articles were put out in the 2010s (35%). Citations per article ranged from 30 to 253. China possesses the most papers among the top 100 papers, followed by the USA, France, Israel and Italy. The study theme that most highlighted were operative hysteroscopy and adjunctive treatments for improving reproductive outcome. Level II is the most common level of evidence, and there is no statistical difference in the number of citations between the levels. The network analysis connoted that hysteroscopy, hysteroscopic adhesiolysis, infertility, and reproductive outcome had a great degree of centrality in the 2000s and 2010s, while placental implantation had a great degree of centrality in the 2000s and stem cell and fibrosis had a great degree of centrality in the 2010s.

Conclusions: We conducted a bibliometric analysis of the top 100 most cited articles in the literature on intrauterine adhesions. It is worth noting that hysteroscopy and hysteroscopic adhesiolysis were long-term concern in the field of intrauterine adhesion researches. As the elapse of time, postoperative adjuvant treatment has gradually become the hot spot of researches. However, there are only 9 experimental articles among these 100 articles, showing the lack of breakthrough progress in the field of intrauterine adhesions at the mechanism level.

Background

Intrauterine adhesion (IUA) was first defined and reported by Asheman Joseph G in 1950 (1, 2). IUA is caused by mechanical injury or infection hurt to the basal layer of the endometrium, resulting in the formation of fibromuscular or severe connective tissue adhesion of the uterine cavity or cervical canal (3, 4). Hypomenorrhea/ amenorrhea (5), infertility(6), recurrent pregnancy loss (7) and obstetric complications (8) are common complication of IUA. IUA may also lead to low birth weight (9). At present, IUA have become one of the stubborn diseases that seriously affect the reproductive prognosis and quality of lives of women in childbearing age (6, 10).

Surgical treatment is the first choice for IUA. Hysteroscopic adhesiolysis, the standard treatment for IUA, hold the limited therapeutic effect though (11). The conception rate is 25% after hysteroscopic adhesiolysis, and the rate of reformation of adhesions is 20%-63% (12–15). In order to reduce the recurrence rate of IUA and improve reproductive prognosis, it is often recommended to assist other prevention and treatment measures for comprehensive management of adhesions after the surgery (16–18). These measures mainly include devices to keep opposing endometrial surfaces separated, such as intrauterine device (IUD) (19), Foley catheter balloon (20), auto-crosslinked hyaluronic acid (ACP) gel (21–24), and interventions to promote endometrial regeneration, such as estrogen (25, 26), stem cell (27–29), stem cell exosome (30), amniotic epithelial cells (31), granulocyte colony stimulating factor (32), platelet rich plasma (33), aspirin (34), etc. However, current effectiveness is still not ideally. The reformation rate is still as high as 48% (35), the conception rate is about 44.3%, and the live birth rate is 37.8% (36). Therefore, when it comes to IUA, how to reduce the reformation rate of IUA and increase the postoperative conception rate and live birth rate is still the main focus of research.

The aim of this research is to figure out and analyze the 100 most cited essays in the field of IUA, emphasize the research trends and hotspots in this area, and evaluate the research quality and properties of the most cited original papers in the past 70 years. This analysis are supposed to provide some guidance for subsequent research directions.

Methods

Results

We extracted 100 articles which is cited most in the field of IUA which is listed in Table 1. Citations ranges from 30 to 253 in number, with a majority of them published in the 2010s (35％) and 2000s (29％). The overall trend was increasing year by year (Fig. 2). In 2008, the number of journals reached highest (n=7). The number of citations was 6462 generally, 47 (0.7%) in the 1960s, 356 (5.5%) in the 1970s, 721 (11.2%) in the 1980s, 1190 (18.4%) in the 1990s, 2097 (32.5%) in the 2000s, and 2051 (31.7%) in the 2010s. The Mann-Kendall trend test showed no time-dependent trend in the publication time of articles (P=0.4654) but an increasing trend between the citation density and the time (P=2.2E-16) (Fig. 3). The Spearman rank revealed a positive correlation between time and citation density (r=0.836, P <2.2E-16). The Shapiro-Wilk test and the Kolmogorov-Smirnov test both indicated an abnormal distribution of the citation data. The Shapiro-Wilk test indicated significant departures from normality (p<0.05) for all distributions tested.

Tab. 1

List of the 100 top-cited articles in intrauterine adhesion research

These articles were distributed in 22 countries (Fig. 4), led by China (n=19) followed by the USA (n=18), France (n=8), Israel (n=8), and Italy (n=8). The allocation is presented on the world map (Fig. 5). In terms of regional distribution, most of the articles published from two countries: America and Asia. The rest were scattered in Europe, Africa and Oceania. Developed countries accounted for 67% of all countries mentioned above. Articles were all published in 33 journals, among which 27 articles were published in "Fertility and sterility", followed by "Human Reproduction" (n=16), American journal of obstetrics and gynecology" (n=6), "Journal of Minimally Invasive Gynecology" (n=5). (Table 2).

Tab. 2

Journals of the 100 top-cited studies published.

Among the 100 highly cited articles, 10 researchers have more than two articles which is listed in Table 3. These authors’ articles are all clinical studies related to IUA. Among them, CM March and Jehn-Hsiahn Yang had 3 fist authorships mainly in the field of IUA. CM March’s focus was on hysteroscopic adhesiolysis, and Jehn-Hsiahn Yang’s research direction was endometrium regeneration. Although R F Valle from the United States had only two articles, the number of citations is relatively high, with an overall number of citations of 286. Auxiliary diagnosis of IUA is his main focus.

Tab. 3

List of first authors with frequent articles within the top-cited list.

The 100 most cited articles mainly focus on the following themes: auxiliary treatment of IUA (n = 28), prognosis of IUA (n=19), incentive factors of IUA (n=16), hysteroscopic adhesiolysis (n=14), evaluation methods for IUA (n=12), complications of IUA (n = 6), relevant mechanism of IUA (n = 4), new devices for IUA (n=1). The most mentioned theme was the adjuvant treatment of IUA, followed by the reproductive prognosis of patients after hysteroscopic adhesiolysis (Fig. 6). One-way ANOVA revealed no significant difference in citations per article among the various themes (Fig. 7). Nevertheless, the impact factor of article from different themes was statistically different (P=0.012) (Fig. 8).

In terms of the level of article evidence, the level II (n=39) category has a mean number of 69 ± 48 citations per article, making up the largest number. The level I (n=23) category has a mean number of 63±30 citations per article, the level IV (n=14) with 48±22 citations. Difference in citations per article between different levels of evidence is not significant analyzed by one-way ANOVA (Fig. 9).

Network analysis of the key words or subject terms has been done in two periods of article published time: in the 2000s (34 articles) and in the 2010s (30 articles). The result indicated that "hysteroscopy", "hysteroscopic adhesiolysis", "infertility", and "reproductive outcome" possessed a high degree of centrality in the 2000s and 2010s, while "placenta accrete" were greatly centralized in the 2000s and "stem cell" and "fibrosis" was highly concentrated in the 2010s (Fig. 10-11).

Discussion

This is the first bibliometric analysis of papers in the field of IUA. Mass of interesting findings can be drawn from this analysis of the top 100 most cited papers published on IUA in the past 70 years. Not only the papers which had made important contributions to the progress in this field were reflected, but also current development trend was revealed. Generally speaking, with the time goes by, the number of citations of papers would be piled up. However, it is contrary to expectation that the number of articles was gradually increasing as time progresses when we assessed the certain 100 most cited articles according to the division of each decade. Articles in 2010s possessed the highest proportion, reaching 35%. As time increases, not only the proportion of articles presented an growing trend, but also the citation density, that is, the number of citations divided by the number of years of publication, figured an increasing trend. On the one hand, this reflects the "obliteration by incorporation" (39), that is, the citations of the original work decreased with the passage of time for familiarity during the long-term and widespread use, and new findings replaced them. On the other hand, this also presented the phenomenon that the diagnosis, treatment and advanced researches related to IUA have been paid more and more attention by the international community. In addition, 91% of these articles were clinical studies, and only 9% were basic experimental studies. Those basic studies mentioned above were all published in the 2010s. We may say that clinical research has always been the focus of researchers in the field of IUA. However, the disease mechanism is also crucial to the treatment of the disease. Current researches on the mechanism had an increasing trend, and it has the potential to provide clinical directions in the future.

Different from the trend of other bibliometric analysis reports, articles originating from the United States and developed countries did not have an absolute advantage. China and the United States were both important sources of articles, with 19 and 18 articles respectively. 33% of the 100 most cited papers were from developing countries, 67% were from developed countries. There are several reasons for this condition: (1) The clinical manifestations of IUA were first reported in the United States in the 19th century, and later defined and named by American doctors. Therefore, they were able to study it earlier and more systematically (40);The United States and other developed countries had sufficient funds to support scientific research. The sharing of these research results will help the progress of researches on IUA (41, 42); (2) As we all know, the occurrence of IUA is closely related to abortion and curettage. Honestly, abortion is considered illegal in many developing countries due to religious beliefs. In developed countries, the rate of abortion dropped by 19 percentage points from 1990 to 2014, while it only fell by 2 percentage points in developing countries (43). Moreover, least-safe abortions accounted for the largest proportion in developing countries (44); (3) China and other developing countries had great population. Propaganda and popularization of contraceptive measures were inadequate. It was inevitable to choose surgical abortion after unintended pregnancy. Repeated or informal intrauterine operations may finally lead to irreversible hurt to endometrium (45, 46); (4) After China opened up the two-child policy, more and more IUA were discovered, and recurrent IUA need to be treated (47, 48). IUA is a universal disease, but unfortunately, no multinational cooperation work was found in these 100 most cited papers.

Actually, the impact factors of journals were not high. This was because related papers were rarely published in comprehensive journals, while the impact factors of obstetrics and gynecology professional journals are relatively low. This result highlighted a growing tendency that researchers may prefer to publish articles in influential professional journals. However, there was no denying that the value of IUA researches have not been highly appreciated.

Nearly 50% of the certain 100 papers were issued in two journals, “Fertility and sterility” and “Human Reproduction”, followed closely by two heavyweight journals in the field of obstetrics and gynecology, “American journal of obstetrics and gynecology” and “Obstetrics and Gynecology”. This demonstrated that IUA were particularly concerned in the field of reproductive medicine. Among the 100 most cited articles, the themes of papers published in recent years appeared to be more diverse, including the Phase I clinical study of autologous stem cell transplantation for the treatment of IUA published in Stem Cell Research & Therapy (49), and collagen scaffold for endometrial regeneration published in Biomaterials (50).

When it comes to the first author of the 100 most cited papers, we found that 2 researchers contributed 3 articles. One of them was Charles M. March from the United States. His articles were all published before 1990, and emphasized that hysteroscopy is the gold standard for diagnosis and classification of IUA, and hysteroscopic adhesiolysis is the first choice for the treatment of IUA (51–53). The other one was Jehn-Hsiahn Yang from Taiwan, China, a younger generation of researchers. The similarity with Charles M. March was that they both focus on hysteroscopy. His three articles have proposed that IUA was common complications after transcervical resection of multiple apposing submucous myomas (54), the formation of new adhesions after hysteroscopic adhesiolysis was the reason that affects endometrial repair (55), the location and area of adhesions were important factors that affect the recurrence of IUA (15).

The level of evidence was between I and V. The overall distribution was average, and level II was relatively high, which is distinct with other bibliometric-related studies. This may attribute to the design of clinical trials. Treatment of IUA was closely related to patients’ reproductive prognosis, and for women, age was also a significant factor. Therefore, considering the effect of placebo control on patients, experimental studies are mostly unilateral. In the future, with the increase in the demand for childbirth and the introduction of two or even three-child opening policies in some countries, it is expected that hysteroscopic adhesiolysis, postoperative adjuvant treatment and related research articles will increase more rapidly.

We also studied the theme distribution of articles. The adjuvant treatment of IUA ranked first, followed by the prognosis of reproductive outcome after hysteroscopic adhesiolysis, the incentive factors of IUA, hysteroscopic adhesiolysis and the evaluation method of IUA. Hysteroscopic adhesiolysis is the primary treatment method. However, how to improve the therapeutic effect through drugs and biological agents after the surgery has been a problem that researchers want to overcome in recent years (56). Network analysis of the author’s key words or subject terms has been done in two periods of article published time: in the 2000s (34 articles) and in the 2010s (30 articles). The result indicated that “"hysteroscopy, hysteroscopic adhesiolysis, infertility and reproductive outcome" was highly centralized in both 2000s and 2010s and placental implantation was highly concentrated in the 2000s. This was consistent with the research trend in recent years. Researchers have gradually realized that even if patients with IUA succeed in conception, there would be many risks of pregnancy complications. The most cited article in this study was also an article about IUA complications, in which the author proposed that patients with IUA were associated with many risks during pregnancy. An analysis of the citation density of papers published in the 2010s, we found each theme was evenly distributed. In the analysis of the impact factor under each theme, it could be seen that articles related to devices and materials were relatively high, while researches on mechanism were relatively low. Stem cell and fibrosis were highly concentrated in the 2010s. In recent years, researchers have paid more and more attention to the effectiveness of adjuvant therapy after hysteroscopic adhesiolysis in suppressing reformation of adhesion and promoting endometrial regeneration (57). Previous researches focused on placement of uterine stents, foley catheters, hyaluronic acid or hormone replacement therapy (58). Nevertheless, more importance was attached to biotherapy, especially in the field of stem cell therapy. Bone marrow mesenchymal stem cells (BMSC) (59), umbilical cord mesenchymal stem cells (UCMSC) (60), and menstrual blood mesenchymal stem cells (MbMSC) (61, 62) have been used clinically in patients with IUA, resulting in an improvement in reproductive outcome. Researchers reported that the stem cells can promote endometrial cells proliferation, especially inhibit the process of fibrosis (63). In 2020, a review brought together the controversies of different researchers on the treatment of IUA (64). One believed that the adjuvant treatment after the surgery should be paid attention to, and another believed that IUA should be treated with multiple operations. However, it cannot be ignored that, hysteroscopic adhesiolysis has always been the center of research over the years, and the discussion of surgical methods and surgical techniques was still a vacancy (65) It is undeniable that the combined effective adjuvant treatment after surgery is the trend of IUA treatment.

This analysis does generate some valuable information, but it still has some restrictions. First of all, the citation analysis was mainly based on Web of Science. The number of citations may be misleading. Meanwhile, we may miss some important papers that were not included in the SCI database. Secondly, we may overlook the newly published articles that were meaningful in this area but have yet to reach high citation levels owing to the criterion that papers were sorted by the number of citations. All in all, it was by no means exhaustive, but the list of most cited articles still includes many influential papers in the field of IUA.

Conclusion

This article highlights the top 100 most cited articles in the IUA over the last 70 years, including their publication time and regional centers, first author, level of evidence, as well as their research theme. We revealed the spotlights and properties of studies about IUA since 1950 to 2020. Furthermore, this article sheds light on the notion that postoperative adjuvant therapy played a key role in the field of IUA, and more and more basic and clinical studies are exploring suitable and effective adjuvant treatments for IUA. Meanwhile, the method and techniques of surgical therapy is also controversial. However, the current prognosis of IUA was extremely poor. The tough problem still remains to be solved. Researchers extremely focused on the clinical trial rather than the basic laboratory research. Thus, the foremost difficult is to conquer the situation that little is known about underlying mechanisms of adhesion formation in the uterine and influencing factors.

Abbreviations

IUA: intrauterine adhesion

IUD: intrauterine device

ACP: auto-crosslinked hyaluronic acid

BMSC: bone marrow mesenchymal stem cells

UCMSC: umbilical cord mesenchymal stem cells

MbMSC: menstrual blood mesenchymal stem cells

Declarations

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Availability of data and materials

Not applicable

Competing interests

The authors declare that they have no competing interests.

Funding

This study was supported by the National Key Research and Development Program of China (grant no. 2018YFC1004800).

Authors' contributions

DX contributed to the design of the study and revise the manuscript. PG and WL contributed to the process of searching, selecting and drafting the manuscript.

Acknowledgements

Not applicable

Footnotes

Not applicable

References

1. Asherman JG. Traumatic intra-uterine adhesions. J Obstet Gynaecol Br Emp. 1950;57(6):892-6.
2. Wang Y, Yao Z, Zhao H, Yue C, Yu Q, Zhang Y, et al. Reproductive Outcomes of In Vitro Fertilization-Intracytoplasmic Sperm Injection after Transcervical Resection of Adhesions: A Retrospective Cohort Study. J Minim Invasive Gynecol. 2020.
3. Hooker AB, de Leeuw RA, Twisk JWR, Brölmann HAM, Huirne JAF. Reproductive performance of women with and without intrauterine adhesions following recurrent dilatation and curettage for miscarriage: long-term follow-up of a randomized controlled trial. Hum Reprod. 2020.
4. Chawla L, Prateek S, Bahadur A, Durgapal P. Intrauterine adhesions with secondary amenorrhea: A notable indicator of endometrial tuberculosis. Indian J Tuberc. 2020;67(4):575-7.
5. March CM. Management of Asherman's syndrome. Reproductive Biomedicine Online. 2011;23(1):63-76.
6. Wang L, Yu C, Chang T, Zhang M, Song S, Xiong C, et al. In situ repair abilities of human umbilical cord-derived mesenchymal stem cells and autocrosslinked hyaluronic acid gel complex in rhesus monkeys with intrauterine adhesion. Sci Adv. 2020;6(21):eaba6357.
7. Diamond MP, Freeman ML. Clinical implications of postsurgical adhesions. Human Reproduction Update. 2001;7(6):567-76.
8. Zhang LP, Wang M, Shang X, Zhang Q, Yang BJ, Xu Y, et al. The incidence of placenta related disease after the hysteroscopic adhesiolysis in patients with intrauterine adhesions. Taiwan J Obstet Gynecol. 2020;59(4):575-9.
9. Baradwan S, Baradwan A, Bashir M, Al-Jaroudi D. The birth weight in pregnant women with Asherman syndrome compared to normal intrauterine cavity: A case-control study. Medicine (Baltimore). 2018;97(32):e11797.
10. Abbott J, Deans R. Accelerating the science after 125 years of treating intrauterine adhesions. J Minim Invasive Gynecol. 2020.
11. Stamenov GS, Vitale SG, Della Corte L, Vilos GA, Parvanov DA, Nikolova DN, et al. Hysteroscopy and female infertility: a fresh look to a busy corner. Hum Fertil (Camb). 2020:1-29.
12. Yu D, Wong Y-M, Cheong Y, Xia E, Li T-C. Asherman syndrome-one century later. Fertility and Sterility. 2008;89(4):759-79.
13. Li C, Cai A, Sun C, Wu B, Chen X, Mao Y, et al. The study on the safety and efficacy of amnion graft for preventing the recurrence of moderate to severe intrauterine adhesions. Genes Dis. 2020;7(2):266-71.
14. Chen L, Zhang H, Wang Q, Xie F, Gao S, Song Y, et al. Reproductive Outcomes in Patients With Intrauterine Adhesions Following Hysteroscopic Adhesiolysis: Experience From the Largest Women's Hospital in China. Journal of Minimally Invasive Gynecology. 2017;24(2):299-304.
15. Yang JH, Chen CD, Chen SU, Yang YS, Chen MJ. The influence of the location and extent of intrauterine adhesions on recurrence after hysteroscopic adhesiolysis. Bjog-an International Journal of Obstetrics and Gynaecology. 2016;123(4):618-23.
16. Doroftei B, Dabuleanu AM, Ilie OD, Maftei R, Anton E, Simionescu G, et al. Mini-Review of the New Therapeutic Possibilities in Asherman Syndrome-Where Are We after One Hundred and Twenty-Six Years? Diagnostics (Basel). 2020;10(9).
17. Di Guardo F, Della Corte L, Vilos GA, Carugno J, Török P, Giampaolino P, et al. Evaluation and treatment of infertile women with Asherman syndrome: an updated review focusing on the role of hysteroscopy. Reprod Biomed Online. 2020;41(1):55-61.
18. Capmas P, Mihalache A, Duminil L, Hor LS, Pourcelot AG, Fernandez H. Intrauterine adhesions: What is the pregnancy rate after hysteroscopic management? J Gynecol Obstet Hum Reprod. 2020;49(7):101797.
19. Huang XW, Lin MM, Zhao HQ, Powell M, Wang YQ, Zheng RR, et al. A prospective randomized controlled trial comparing two different treatments of intrauterine adhesions. Reprod Biomed Online. 2020;40(6):835-41.
20. Yang X, Liu Y, Li TC, Xia E, Xiao Y, Zhou F, et al. Durations of intrauterine balloon therapy and adhesion reformation after hysteroscopic adhesiolysis: a randomized controlled trial. Reprod Biomed Online. 2020;40(4):539-46.
21. Zhou Q, Shi X, Saravelos S, Huang X, Zhao Y, Huang R, et al. Auto-Cross-Linked Hyaluronic Acid Gel for Prevention of Intrauterine Adhesions after Hysteroscopic Adhesiolysis: A Randomized Controlled Trial. J Minim Invasive Gynecol. 2020.
22. Zheng F, Xin X, He F, Liu J, Cui Y. Meta-analysis on the use of hyaluronic acid gel to prevent intrauterine adhesion after intrauterine operations. Exp Ther Med. 2020;19(4):2672-8.
23. Yao Q, Zheng YW, Lan QH, Wang LF, Huang ZW, Chen R, et al. Aloe/poloxamer hydrogel as an injectable β-estradiol delivery scaffold with multi-therapeutic effects to promote endometrial regeneration for intrauterine adhesion treatment. Eur J Pharm Sci. 2020;148:105316.
24. Huberlant S, Leprince S, Allegre L, Warembourg S, Leteuff I, Taillades H, et al. In Vivo Evaluation of the Efficacy and Safety of a Novel Degradable Polymeric Film for the Prevention of Intrauterine Adhesions. J Minim Invasive Gynecol. 2020.
25. Kaczynski P, Bauersachs S, Goryszewska E, Baryla M, Waclawik A. Synergistic action of estradiol and PGE2 on endometrial transcriptome in vivo resembles pregnancy effects better than estradiol alone†. Biol Reprod. 2020.
26. Chang Y, Duan H, Shen X, Wang S, Guo Z, Chen S. Controversy in the management of oestrogen therapy before hysteroscopic adhesiolysis: a systematic review and meta-analysis. Reprod Biomed Online. 2020;41(4):715-23.
27. Li J, Huang B, Dong L, Zhong Y, Huang Z. WJ‑MSCs intervention may relieve intrauterine adhesions in female rats via TGF‑&beta;1‑mediated Rho/ROCK signaling inhibition. Mol Med Rep. 2021;23(1).
28. Xin L, Lin X, Zhou F, Li C, Wang X, Yu H, et al. A scaffold laden with mesenchymal stem cell-derived exosomes for promoting endometrium regeneration and fertility restoration through macrophage immunomodulation. Acta Biomater. 2020;113:252-66.
29. Park M, Hong SH, Park SH, Kim YS, Yang SC, Kim HR, et al. Perivascular Stem Cell-Derived Cyclophilin A Improves Uterine Environment with Asherman's Syndrome via HIF1α-Dependent Angiogenesis. Mol Ther. 2020;28(8):1818-32.
30. Tan Q, Xia D, Ying X. miR-29a in Exosomes from Bone Marrow Mesenchymal Stem Cells Inhibit Fibrosis during Endometrial Repair of Intrauterine Adhesion. Int J Stem Cells. 2020;13(3):414-23.
31. Ouyang X, You S, Zhang Y, Zhang C, Zhang G, Shao X, et al. Transplantation of Human Amnion Epithelial Cells Improves Endometrial Regeneration in Rat Model of Intrauterine Adhesions. Stem Cells Dev. 2020;29(20):1346-62.
32. Lin X, Zhang Y, Pan Y, He S, Dai Y, Zhu B, et al. Endometrial stem cell-derived granulocyte-colony stimulating factor attenuates endometrial fibrosis via sonic hedgehog transcriptional activator Gli2. Biol Reprod. 2018;98(4):480-90.
33. Peng J, Li M, Zeng H, Zeng Z, Huang J, Liang X. Intrauterine infusion of platelet-rich plasma is a treatment method for patients with intrauterine adhesions after hysteroscopy. Int J Gynaecol Obstet. 2020;151(3):362-5.
34. Zhang Z, Li S, Deng J, Yang S, Xiang Z, Guo H, et al. Aspirin inhibits endometrial fibrosis by suppressing the TGF‑β1‑Smad2/Smad3 pathway in intrauterine adhesions. Int J Mol Med. 2020;45(5):1351-60.
35. Amer MI, Abd-El-Maeboud KH. Amnion graft following hysteroscopic lysis of intrauterine adhesions. Journal of Obstetrics and Gynaecology Research. 2006;32(6):559-66.
36. Chen Y, Liu L, Luo Y, Chen M, Huan Y, Fang R. Effects of Aspirin and Intrauterine Balloon on Endometrial Repair and Reproductive Prognosis in Patients with Severe Intrauterine Adhesion: A Prospective Cohort Study. Biomed Research International. 2017;2017.
37. Zhang W, Tang N, Li X, George DM, He G, Huang T. The top 100 most cited articles on total hip arthroplasty: a bibliometric analysis. J Orthop Surg Res. 2019;14(1):412.
38. Borgatti SP, Mehra A, Brass DJ, Labianca G. Network analysis in the social sciences. Science. 2009;323(5916):892-5.
39. Ahmad SS, Ahmad SS, Kohl S, Ahmad S, Ahmed AR. The hundred most cited articles in bariatric surgery. Obes Surg. 2015;25(5):900-9.
40. Schenker JG. Etiology of and therapeutic approach to synechia uteri. European journal of obstetrics, gynecology, and reproductive biology. 1996;65(1):109-13.
41. Khan Z, Goldberg JM. Hysteroscopic Management of Asherman's Syndrome. Journal of Minimally Invasive Gynecology. 2018;25(2):218-28.
42. Cervelló I, Gil-Sanchis C, Santamaría X, Cabanillas S, Díaz A, Faus A, et al. Human CD133(+) bone marrow-derived stem cells promote endometrial proliferation in a murine model of Asherman syndrome. Fertil Steril. 2015;104(6):1552-60.e1-3.
43. Sedgh G, Bearak J, Singh S, Bankole A, Popinchalk A, Ganatra B, et al. Abortion incidence between 1990 and 2014: global, regional, and subregional levels and trends. Lancet. 2016;388(10041):258-67.
44. Cameron S. Recent advances in improving the effectiveness and reducing the complications of abortion. F1000Res. 2018;7.
45. Guo C, Pang L, Wen X, Zheng X. Risky Sexual Behaviors and Repeat Induced Abortion Among Unmarried Young Women in China: Results from a Large, Nationwide, Population-Based Sample. J Womens Health (Larchmt). 2019;28(10):1442-9.
46. Zong Z, Sun X, Mao J, Shu X, Hearst N. Contraception and abortion among migrant women in Changzhou, China. Eur J Contracept Reprod Health Care. 2020:1-6.
47. Jiang Y, Han J, Donovan C, Ali G, Xu T, Zheng Y, et al. Induced Abortion among Chinese Women with Living Child-A National Study. Adv Dis Control Prev. 2017;2(1):10-5.
48. Zeng Y, Hesketh T. The effects of China's universal two-child policy. Lancet. 2016;388(10054):1930-8.
49. Cao Y, Sun H, Zhu H, Zhu X, Tang X, Yan G, et al. Allogeneic cell therapy using umbilical cord MSCs on collagen scaffolds for patients with recurrent uterine adhesion: a phase I clinical trial. Stem Cell Research & Therapy. 2018;9.
50. Lin N, Li Xa, Song T, Wang J, Meng K, Yang J, et al. The effect of collagen-binding vascular endothelial growth factor on the remodeling of scarred rat uterus following full-thickness injury. Biomaterials. 2012;33(6):1801-7.
51. March CM, Israel R. Intrauterine adhesions secondary to elective abortion. Hysteroscopic diagnosis and management. Obstetrics and gynecology. 1976;48(4):422-4.
52. March CM, Israel R. Gestational outcome following hysteroscopic lysis of adhesions. Fertility and sterility. 1981;36(4):455-9.
53. March CM, Israel R, March AD. Hysteroscopic management of intrauterine adhesions. American journal of obstetrics and gynecology. 1978;130(6):653-7.
54. Yang J-H, Chen M-J, Wu M-Y, Chao K-H, Ho H-N, Yang Y-S. Office hysteroscopic early lysis of intrauterine adhesion after transcervical resection of multiple apposing submucous myomas. Fertility and Sterility. 2008;89(5):1254-9.
55. Yang J-H, Chen M-J, Chen C-D, Chen S-U, Ho H-N, Yang Y-S. Optimal waiting period for subsequent fertility treatment after various hysteroscopic surgeries. Fertility and Sterility. 2013;99(7):2092-+.
56. Takai IU, Kwayabura AS, Ugwa EA, Idrissa A, Obed JY, Bukar M. A 10-year Review of the Clinical Presentation and Treatment Outcome of Asherman's Syndrome at a Center with Limited Resources. Ann Med Health Sci Res. 2015;5(6):442-6.
57. Kou L, Jiang X, Xiao S, Zhao YZ, Yao Q, Chen R. Therapeutic options and drug delivery strategies for the prevention of intrauterine adhesions. J Control Release. 2020;318:25-37.
58. Berman JM. Intrauterine adhesions. Seminars in Reproductive Medicine. 2008;26(4):349-55.
59. Santamaria X, Mas A, Cervello I, Taylor H, Simon C. Uterine stem cells: from basic research to advanced cell therapies. Human Reproduction Update. 2018;24(6):673-93.
60. Cao Y, Sun H, Zhu H, Zhu X, Tang X, Yan G, et al. Allogeneic cell therapy using umbilical cord MSCs on collagen scaffolds for patients with recurrent uterine adhesion: a phase I clinical trial. Stem Cell Res Ther. 2018;9(1):192.
61. Chen L, Qu J, Xiang C. The multi-functional roles of menstrual blood-derived stem cells in regenerative medicine. Stem Cell Research & Therapy. 2019;10.
62. Ma H, Liu M, Li Y, Wang W, Yang K, Lu L, et al. Intrauterine transplantation of autologous menstrual blood stem cells increases endometrial thickness and pregnancy potential in patients with refractory intrauterine adhesion. J Obstet Gynaecol Res. 2020;46(11):2347-55.
63. Azizi R, Aghebati-Maleki L, Nouri M, Marofi F, Negargar S, Yousefi M. Stem cell therapy in Asherman syndrome and thin endometrium: Stem cell- based therapy. Biomed Pharmacother. 2018;102:333-43.
64. Santamaria X, Liu JH, Aghajanova L, Isaacson K, Movilla P, Fernandez H, et al. Should we consider alternative therapies to operative hysteroscopy for the treatment of Asherman syndrome? Fertil Steril. 2020;113(3):511-21.
65. Koythong T, Guan X. Consideration for an optimal and practical approach to hysteroscopic adhesiolysis of intrauterine adhesions. Ann Transl Med. 2020;8(11):663.