Bibliometric analysis and global trends in uterus transplantation

Aim: The purpose of this study was to characterize publication patterns, academic influence, research trends, and the recent developments in uterus transplantation (UTx) across the globe. Methods: The Web of Science Core Collection database was searched for documents published from the time the database began to include relevant articles to 15 December 2023. With the use of VOSviewer, Citespace, BICOMB, and Incites, a cross-sectional bibliometric analysis was conducted to extract or calculate the evaluative indexes. Publications were categorized by country, institution, author, journal, highly cited papers, and keywords. The variables were compared in terms of publication and academic influence, which further included citation count, citation impact, Hirsh index, journal impact factor, total link strength, collaboration metrics, and impact relative to the world. Results: A total of 581 papers concerning UTx were initially identified after retrieval, and 425 documents were included. Of the 41 countries participating in relevant studies, the USA and Sweden were in leading positions in terms of publications, citations, and academic influence. The most versatile institution was the University of Gothenburg, followed by Baylor University. The most productive scholars and journals were Brännström M. and Fertility and Sterility, respectively. Five groups of cutting-edge keywords were identified: venous drainage, donors and donation, women, fertility preservation, and fertility. Topics about surgery, first live birth, risk, and in vitro fertilization remain hot in this field. Conclusions: UTx is anticipated to enter a golden era in the coming years. This study provides some guidance concerning the authors involved in promoting UTx research, the current development of UTx, and journals to submit their innovative research. This also helps to reach a comprehensive insight and prospect in the near future. In order to establish recognized standards and benefit more patients who are disturbed by uterine infertility, large-scale and well-designed clinical trials are required.


Introduction
Absolute uterine factor infertility (AUFI) is a major type of female infertility that primarily results from the congenital absence of the uterus, previous hysterectomy, and severe intrauterine adhesion.It is estimated to affect ~100 million fertile-age women around the globe [1] .Historically, women with AUFI have had limited options for motherhood and are restricted to adoption and surrogacy.However, adoption does not establish a genetic relationship between the child and the mother, and surrogacy is not permitted in numerous jurisdictions.In addition, these alternatives may introduce legal, cultural, ethical, and emotional challenges for the family.As a result, novel approaches are desperately needed to address AUFI and advance female fertility.

HIGHLIGHTS
• This study is the first thorough bibliometric analysis of uterus transplantation, which is the only choice for absolute uterine factor infertility.• The USA and Sweden were in leading positions in terms of publications, citations, and academic influence.• The most productive scholar was Brännström M. from the University of Gothenburg, and the most productive journal was Fertility and Sterility.• The cutting-edge keywords were clustered into five groups: venous drainage, women, fertility preservation, fertility, as well as donors and donations.
Since the beginning of the 21st century, uterus transplantation (UTx) has emerged as the only treatment option for AUFI.The Turkish first pregnancy and Swedish first live birth of a healthy baby after UTx demonstrated the feasibility of childbirth via UTx, which inspired reproductive centers across the world [2,3] .Following this breakthrough, similar cases have been reported in the USA, Brazil, France, and China [4][5][6][7] .The progression of UTx has been further propelled by innovative advancements such as the introduction of robotic-assisted surgeries, the establishment of the International Uterus Transplantation Society, and the identification of the outflow utero-ovarian veins.However, UTx is still in its infancy compared to other solid organ transplantations, with just over 80 UTx operations performed in nearly 20 centers globally by 2023 [8,9] .As an innovative surgical method, UTx is worth considerable attention, especially in the context of an aging population and continuously declining fertility rates.
With regard to ethics [10,11] , policy [12,13] , surgical methods [14,15] , and immunity (Fig. 1) [16] , UTx is a complex clinical practice.Although UTx treatment has been reviewed from these aspects, there has been little examination of previous publications, academic influence, and research trends in UTx across the globe.Bibliometric methods have been used to explore the productivity of countries, institutions, and researchers within a given subject area and to identify remarkable events, papers, and future trends.Therefore, by using bibliometric analysis, the publication and researcher performance were examined.It helps experts and newcomers to identify the breadth of their field, locate fresh topics of interest, and develop future research plans visually.

Methods
The institutional review board of the Tongji hospital deemed that ethical approval was not necessary.This study is a cross-sectional observation study, and thus, we followed the reporting guidelines of the Strengthening the Reporting of Observational Studies in Epidemiology [17] .It helps us uphold the highest standards of scientific rigor, objectivity, and replicability characteristic of our manuscript.

Data collection
We used the Web of Science Core Collection (WOSCC) to identify publications of UTx from the time the database began to include relevant articles to 15 December 2023.In order to encompass all the literature pertaining to the research topic while excluding irrelevant documents as much as possible, we conducted a topical search using the query: 'uterus transplantation' or 'uterine transplantation' and human.Retrieved papers were exported with full records and cited references in plain text format.

Selection of eligible studies
The 'plain text' was imported into EndNote X9 for deduplicate.The procedure for data retrieval and collection is shown in Figure 2. It is necessary to conduct a manual screening process in order to identify the final literature to be analyzed.Therefore, the authors (T.W. and Y.Y.W.) independently screened the title and abstract to identify the available studies based on the following criteria.Inclusion criteria were the following: (i) papers focusing on human UTx; and (ii) language was limited to English.Exclusion criteria were the following: (i) irrelevant topics that superficially mentioned UTx (e.g.studies that investigated disorders lead to AUFI but not treatment); (ii) studies conducted only on animal models and no human experiments or work have been conducted; and (iii) papers with missing information (e.g.author details, journal name, or publication year).We set no restrictions for study design (e.g.observational, experimental) or type of publication (e.g.editorial, original article, review).Discrepancies between selected studies by both authors were discussed in a consensus meeting, with the senior author (J.J.Z.) giving a binding verdict.

Data extraction, standardization, and analysis
The VOSviewer 1.6.18 was used to cluster the countries/ regions, institutions, and journals.The Citespace 6.2.4 was used for visualizing the authors' network, generating keyword maps, and conducting burst word analysis.Most importantly, synonymous expressions were standardized manually to eliminate redundant entries.For instance, 'uterus transplantation' and 'uterine transplantation' were merged.The BICOMB 2.0 was used to perform a co-occurrence matrix of high-frequency keywords, and then gCLUTO was used to generate a matrix visualization and a mountain visualization.In addition, the GraphPad Prism 8.0 was used to perform the statistical analyses.The country's level of income was determined according to World Bank data for 2023.

Academic influence measurement
Academic influence is a master criterion for assessing the academic excellence of the document, journal, institution, researcher, etc., and its measurement is inherent and diverse.We used the combined metrics to measure academic influence (Table 1).

Baseline characteristics of the eligible documents
A total of 581 publications were initially retrieved from the search (Fig. 2).After excluding studies that were duplicated, irrelevant, and restricted to animal models (n = 152), a total of 425 documents were identified as eligible studies.These documents encompassed several types of publications, with original articles constituting 48.47% and reviews accounting for 19.06% (Fig. 3A).Moreover, 16.00% of the publications included editorials, indicating that there is a recognized significance for UTx.Interestingly, UTx received little attention until 2013, with no more than six papers published annually (Fig. 3B).However, the number of publications per year has shown a consistent increase since 2013 and will reach a peak of 60 publications in 2021.A similar pattern was also observed in the number of citations, which began to increase in 2016 and peaked at 1537 in 2021 (Fig. 3B).The citation impact displayed a slightly increasing trend from 2001, with a noticeable increase in 2009 and 2010 (Fig. 3C).When adjusted for the year, the citation per year demonstrated a continuous increase in the past 5 years (Fig. 3C).With regard to the involved research areas, over half of the papers (n = 217, 51.06%) belonged to the Obstetrics Gynecology (OB/GYN) category, followed by Reproductive biology (n = 88, 20.71%), Transplantation (n = 70, 16.47%), Surgery (n = 59, 13.88%), and Ethics (n = 44, 10.35%) (Fig. 3D).However, the most citations were given to social issues and surgery (with an impact of 3.0 and 2.4, respectively), indicating their consistent public interest.Taken together, UTx is an interdisciplinary field involved in medicine, ethics, and sociology that is developing rapidly at the moment.

History of UTx
There are some chronological key events in the history of UTx that promoted its development since its inception (Fig. 4).In April 2000, after performing UTx in baboons and goats, Fageeh et al. [18] in Saudi Arabia reported the first human UTx, which ended in the removal of a necrotic uterus 99 days later.They concluded that UTx is feasible and safe and that, to implement the discipline in human clinical practice, surgical, vascular anatomy, and strong fixation are necessary.However, there was a 10-year silence on UTx following the first case.Until 2011, surgeons from Turkiye performed another UTx operation using a donated uterus from a brain-dead, 22-yearold female [19] .The woman achieved the first pregnancy after embryo transfer, but ended in chemical pregnancy [3] .Afterward, clinical trials involving live donors (LDs) or deceased donors (DDs) were approved and initiated [2,5,20] .UTx completed the mission for AUFI in 2014.For the first time, a live birth was reported after UTx in Sweden, and it  Papers that contain one or more international co-authors Impact relative to the world Citation impact of the set of publications as a ratio of the world average Highly cited paper (HCP) Top one percent in each of the Essential Science Indicators subject areas per year  provided detailed references on patient selection, surgical steps, immunosuppression strategy, etc [2] .Although cesarean delivery was undertaken in 32 weeks, the first postnatal week of the newborn was uneventful, indicative of being normal for gestational age.The first live birth following UTx from a DD was reported in a patient with Mayer-Rokitansky-Küster-Hauser syndrome in Brazil [21] .In 2015, Dr Wei at Xijing Hospital in China performed the world's first robot-assisted donor surgery.The operation took only 6 h, which is much shorter than previous studies [6] .In January 2016, the International Society of Uterus Transplantation was founded and comprised of world experts and pioneers dedicated to the development of UTx.In recent years, UTx or live births have been achieved in many countries or regions, and the processes were similar to those of prior studies.

Distributions of countries
Forty-one countries contributed to the global discourse, of which 63.41% were high-income countries, 19.51% were upper-middle-income countries, and 17.07% were lowermiddle-income countries (Fig. 5A, Table 2).The geographical distribution of the global productivity map showed that most research publications on UTx originated from European, North American, and Asian nations.The involved countries were grouped into four clusters, indicating diverse regional distribution patterns, possibly stemming from the collaborative relationships among these nations (Fig. 5B).As a result of their high productivity levels, citations, and H-index, the USA and Sweden have been identified as the leading contributors to UTx research (Fig. 5C).The USA had the highest international (value = 55), domestic (value = 49), and industry collaborations (value = 1), highlighting the extensive nature of its collaborative efforts (Fig. 5D).Spain registered the highest indicator (value = 4.28) in terms of impact relative to the world, followed by Australia (value = 3.96).

Participants of institutions, authors, and highly cited papers
The top 10 institutions that published the most papers on human UTx are presented in Table 3.With the highest number of publications (n = 85) and citations (n = 2818), the University of Gothenburg in Sweden distinguished itself as an influential contributor to scientific research.The VOSviewer revealed that the University of Gothenburg and Baylor University were representative institutions in their respective countries (Fig. 6A).Moreover, these two organizations worked closely with both domestic and foreign academic institutions.Among the 1083 authors included, the most prolific authors in the bibliometric analysis were Brännström M. (n = 73), Johannesson L. (n = 66), and Testa G. (n = 46) (Table 4).Brännström M. and Johannesson L. had equally strong link strength with other authors (value = 180).They were also the top two researchers who cooperated with international and domestic partners.Olausson M. (value = 3.28) and Kvarnström N. (value = 3.90) were the top two in terms of the impact relative to the world.Both of them worked at the University of Gothenburg, the same as Brännström M. The centralized author clustering suggested close collaborations among these authors (Fig. 6B).Table 5 shows the top 10 The first clinical outcomes of UTx in different aspects have been reported in most studies.For instance, Brännström M. et al. [2] documented the first live birth through UTx, accumulating 500 citations.Notably, the HCPs were predominantly produced by the aforementioned top institutions and authors in the field.

Descriptions of the source journals
The top 3 academic journals out of 121 were Fertility and Sterility (n = 48; Table 6), BJOG -An International Journal of Obstetrics and Gynaecology (n = 26), and Transplantation (n = 19).The journal with the highest impact factor was the Lancet (JIF = 168.9),followed by the American Journal of Bioethics (JIF = 13.4).Moreover, these relevant journals were categorized into three groups based on their co-citation relationships (Fig. 7A).

Keywords of research hotspots
Keywords play a critical role in reflecting the central messages, areas of interest, and future directions of a discipline.Overall, 980 key terms were retrieved from the titles and abstracts.
Table 7 shows the top 20 keywords, which identify established themes such as uterus transplantation, pregnancy, and infertility, as well as uncharted territory, including follow-up, Montreal criteria, and quality of life within the field of study.Figure 8A displays the keywords grouped into five clusters, each represented by a different color.It revealed the importance of the vascular anastomosis procedure (venous drainage), donor selection and surgery (women, and donors and donation), and fertility strategies (fertility preservation and fertility).This study demonstrates further the strength of keyword bursts as a crucial indicator of the study frontiers.Most significantly, the citation   8B). Figure 8C shows the visualization matrix of the high-frequency keywords.Mountain visualization was used to verify the effect of the visualization matrix, with each mountain representing a cluster (Fig. 8D).

Discussion
Global performance in the human UTx The current cross-sectional bibliometric analysis performed the status and trends in human UTx research.The results showed that in the last 10 years, particularly since the first live birth following UTx, there has been a significant increase in attention to UTx, and it is experiencing the best of times.It is perhaps that UTx is unique in permitting LD transplantation and for reproductive use.Overall, 425 papers in this field were identified, and 14 milestone events were summarized.Despite the overall volume of research being low, as UTx progressed, more countries are believed to have live births via UTx over time.In particular, the USA, which has contributed the highest number of publications, and Sweden, which has garnered the most citations, have developed a competitive environment.However, there is a decreasing trend in the number of studies from these two countries, while research output from other nations is on the rise.Brännström, M. from the University of Gothenburg, has become the most prolific publisher in the field, and he has also collaborated with other institutions, contributing to the first UTx cases in the Middle East and Australia [22,23] .

Multidisciplinary research status of UTx
The OB/GYN type accounts for most publications and many more researchers are engaged in UTx from the OB/GYN standpoint.This predominance is justified because UTx is not merely a surgical procedure but a long-term medical management that also covers various OB/GYN aspects, such as in vitro fertilization, gynecological surgery, embryo transfer, and pregnancy monitoring.Notably, multidisciplinary researchers must work together to further enhance UTx.Johannessona et al. [14] suggested that any center implementing a program for UTx should have an established abdominal transplant program, a gynecologic surgery program, a highrisk obstetric and neonatal care, and an institutional support and oversight.Therefore, a successful UTx program requires broad support from various specialties starting with initial patient referral to delivery and follow-up of the child.
In addition to clinical factors, key unresolved issues related to ethics, policy, and immunity also need to be addressed (Fig. 1).For example, who owns and controls the transplanted uterus before and after UTx?As the graft is a transitory organ, it will be removed again after one or two live births.And then, to whom does the uterus belong since it may in theory be implantable in another recipient? [24]Another important question involves the motivation for patients with AUFI to undergo UTx rather than choose adoption or surrogacy.It The first reporting a live birth after mother-to-daughter UTx, and it also represented the second birth ever after human UTx could have to do with the cost, adoption qualification, privacy, experience of gestation, and psychological desire for a biological relationship [25] .

Country-level productivity and collaboration
There are currently no reports of UTx studies conducted in any low-income countries.This is in line with the observation that the poorest third of the world's population receives only 3.5% of the estimated 234 million major surgical operations undertaken worldwide [26] .The lack of access to surgical care and the lack of surgical necessity, which also applies to UTx, is a result of this vast decline in low-income countries.Barriers may exist in, but are not limited to, the requirement for highly skilled surgical procedures, insufficient research funding, lack of research infrastructure, shortage of awareness, and traditional beliefs about disease processes [27] .Currently, achieving UTx in resource-limited settings is challenging.It is important to strengthen the general healthcare level and basic surgical system in these regions [28] .
The USA and Sweden are the most active countries in the field, with their dominance attributable to their bold innovation and practices, as reflected by a number of initial clinical reports on various aspects of UTx.Other factors contributing to the development of UTx include lower labor costs, fewer regulatory barriers, and a greater number of potential participants.However, there is an ongoing debate regarding whether UTx should be conducted, particularly given that The circulation only contains reviews and articles.JIF, journal impact factor.altruistic surrogacy is legally permitted in certain regions [29] .UTx is expected to serve a wider demographic, including transgender male-to-female individuals and cis-gender males.Such cases are more likely to initially emerge in Western countries due to cultural and policy differences.Interestingly, the development of UTx in some countries necessitates support from the top-cited countries.The first UTx Czech clinical trial was in collaboration with Olausson, M., who ranked eighth among the top productive authors [30] .The first live birth following UTx in the Middle East was a result of Swedish-Lebanese-Jordanian cooperation [23] .Since 1998, the Swedish and Australian teams have established a close relationship, and this contributed to the first Australian UTx procedure [22] .According to the results of an online survey, 62.4% of healthcare providers had heard of UTx, most of whom had heard about it through social media or a news source, but only 17.9% of providers agreed that UTx was relevant to their clinical practice [31] .Professional continuing medical education on UTx is therefore necessary and beneficial.The Swedish team has provided support and training for teams planning UTx procedures internationally [22] .A systematically organized and effective continuing medical education curriculum should encompass qualified faculty, definitive objectives, and methodological details, among other components [32] .Furthermore, telesurgery has emerged as a potential alternative that may advance UTx surgery and provide benefits including reduced costs, enhanced performance, and convenience [33] .In the meantime, the formation of the International Society of Uterus Transplantation and the ethical and reporting guidelines are great approaches to promote the communication and development of UTx.

Evolutionary trend of HCPs
The top two HCPs reported the first live birth resulting from UTx and the first case of UTx, respectively.However, the former was published in the Lancet (JIF = 168.9),while the latter appeared in the International Journal of Gynecology & Obstetrics (JIF = 3.8).This significant gap in JIF could be linked to a potential publication bias against negative results prevalent at that time [34] .Negative trials, however, are equally important since they provide insights into the shortcomings of a procedure.Consequently, the first UTx operation holds equal scientific significance because it underscored the importance of uterine fixation, prompting subsequent improvements to address concerns about compromised blood supply [35] .Similar to this, the first pregnancy after UTx was achieved in a 21-year-old female by Ozkan's team, but the patient experienced five failed pregnancies afterward [19] .An obstructed blood outflow was observed under the perfusion computed tomography, and so a revision surgery was conducted [3] .This is the first case in which additional revision surgery resulted with a live birth, and it also stressed the important of a thorough imaging examination.

Discussion on the study of research hotspots
Keyword analysis elucidates the current frontiers in the human UTx field and reflects a trajectory that is in tandem with the rapidly advancing age.This landscape is sculpted by emergent technological innovations and shaped by the demands of an increasingly deserved fertility preservation.

Vascular anastomosis
The inflow and outflow of the grafts are established via several uterine arteries and venous pedicles, respectively.Arterial anastomosis is performed with or without anterior division of the internal iliac artery to the external iliac artery of the recipient end-to-side (Fig. 9).In terms of veins, the uterine veins or utero-ovarian veins of the LD graft are anastomosed either separately to the external iliac veins in an end-to-side fashion or the utero-ovarian veins are anastomosed to the graft's uterine veins, which are anastomosed together to the external iliac veins.With a DD graft, uterine veins are usually anastomosed using a segment/patch of the internal iliac veins [36] .The procured venous pedicles of the first UTx case were elongated by segments of the great saphenous vein and anastomosed to the external iliac veins.Using finer 8-0 Prolene sutures instead of running 7-0 Prolene is another way to improve vein drainage [5] .In addition, a Doppler probe can be secured to one of the uterine arteries to monitor flow in the immediate postoperative period.

Venous drainage
Correct and efficient venous drainage is necessary to produce a competent uterus that does not show signs of venous congestion, thus facilitating the complete survival of the transplanted tissues.Much drainage of the uterus relies on the deep and superficial uterine veins, with the ureter as the boundary.The former consists of two to six veins on each side and further forms plexuses and ends in the internal iliac vein [37,38] .Dissecting the deep uterine veins is, however, the most demanding part of LD hysterectomy because these veins may be located both ventrally and dorsally to the ureter, making it difficult to procure the graft without damaging the ureter, tiny veins, and nervous plexuses [39] .Poor preoperative imaging and great interindividual and intraindividual variations in number and caliber between and among individuals may cause the disease to worsen.Nevertheless, it is still feasible to obtain long vascular pedicles, including part of the internal iliac veins, without compromising postoperative recovery in LDs (Fig. 9) [40] .Another solution is to divide one of the uterine veins first and reanastomose the divided veins at the back table [40,41] .
Complete utero-ovarian veins may also serve as venous outflow.As demonstrated by Testa et al., the use of utero-ovarian veins was safer and easier (Fig. 9).Some teams have also performed UTx with drainage achieved exclusively using uteroovarian veins and/or ovarian veins [6,42,43] .A normal pregnancy could be sustained solely with utero-ovarian veins, regardless of the uterine veins.It should be noted that bilateral oophorectomy should not be performed in cases of preterm ovarian insufficiency in premenopausal LD.A hazard ratio of 1.41 for all-cause mortality in women younger than 50 years with versus without bilateral oophorectomy was reported.However, there have been reports of uterine and ovarian vein retrievals (including oophorectomies) from premenopausal LD, which led to primary ovarian insufficiency [6,43] .

Donors and donations
Deceased donation is the standard of care to overcome organ shortage in most developed countries.Most notably, it excludes the surgical risks of LDs, costs less time and energy, and provides optimal uterine vessels (Table 8).Rapid and less extensive donor screening shall generally be carried out within 24 h of the UTx procedure in the event of a planned DD procedure.The ureter can be directly transected in DDs, and the procurement duration is shorter than that in LDs.Internal iliac vessels, along with uterine vessels, are dissected caudally from the common iliacs.All branches from the internal iliacs, except the uterine vessels, are ligated and divided [9] .In 2011, the first UTx from a DD was conducted in Turkeyi, which resulted in pregnancy, but the gestation ended in miscarriage [20,44] .There are controversies with regard to the timing of uterine procurement in relation to the procurement of other organs.If the uterus is excised as the first organ, the cold ischemia times of the other grafts are extended [45] .The uterus can also be retrieved at the very end of a multiorgan retrieval, and this would vice versa prolong the cold ischemia time of the uterine graft [46] .

Surgical technique
The classical surgical technique of uterine procurement in LDs is laparotomy, whereas conventional laparoscopy and roboticassisted laparoscopy are gradually transforming transplantation surgeries.Minimally invasive surgeries are commonly used for hysterectomy, lymphadenectomy, and myomectomy within the field of gynecological surgery.The first case via minimally invasive surgery in UTx included a fully robotic retrieval of the uterus within an LD UTx trial, where a premenopausal mother donated her uterus to her daughter with Mayer-Rokitansky-Küster-Hauser syndrome.Similar to the advantages possessed by traditional robotic surgery, it also shows improvements in terms of three-dimensional optics, camera stability, absence of tremors, and expedited learning curves during UTx [47,48] .Furthermore, using robotics in donor UTx reduces the operation duration (4 h compared to 14 h in the Swedish cases), which allows for greater precision in complex dissection procedures.Taken together, robotic-assisted laparoscopy is a promising technique for donor hysterectomy during UTx.It should be noted that this is a robotic surgical procedure in its infancy and that surely developments will take place within the coming years.These advancements will most likely lead to better outcomes for LDs and recipients.As previously mentioned, it is quite likely that in the relatively near future, most LD UTx cases will be performed by roboticassisted surgery in both donors and recipients.

Strengths and limitations
This study has several strengths.First, to the best of our knowledge, this study is the first bibliometric analysis to comprehensively describe the up-to-date development of UTx.It helps OB/ GYN scholars to understand the pioneering groups, collaboration patterns, and journal performance in the UTx domain [49] .Second, this study employed fractional counting instead of full counting, which facilitates the normalization of fields and accounts for the confounding effects arising from the aggregation of substantial studies.Third, the assessment of journal performance is not confined to the conventional JIF metric, which solely reflects the journal's numerical value rather than that of its individual articles.Other metrics, including the H-index, JIF, and total link strength, have also been included for a more comprehensive assessment.
Certain limitations have also been noted in this study.First, it is important to acknowledge that our analysis was solely based on the WOSCC, but this question is inherent to any bibliometric approach.Although this database is comprehensively updated daily and contains a large volume of literature, we are confident that the results achieved in this study are a true reflection of the UTx literature.Comparing results from other databases could be useful for future research; however, this was outside the scope of our current study.Second, although we used the Journal Citation Reports categories to define research fields, these categories do not classify studies in detail.For example, OB/GYN includes a very broad range of highly cited studies.A more detailed classification may be appropriate for a closer look at research trends.Third, while our study identified trends in UTx research, it is important to recognize that it offers a broad overview rather than an in-depth analysis.Several intriguing aspects were not thoroughly explored, including the optimal timing of assisted

Conclusion
UTx is expected to enter a golden era in the coming years after improvements in vascular anatomy, surgical experience, and minimally invasive surgery.It has learned a lot from advancements in the fields of reproductive medicine, transplantation, obstetrics, and gynecology.Most principles of the latter are well established, and minor modifications are required to apply standard practice in UTx.Additionally, UTx has gained global collaboration and has met new challenges.

Figure 1 .
Figure 1.Multidisciplinary characteristics of human uterus transplantation (UTx) and questions in each research areas that are in need of additional evidence to address.DD, deceased donor; IVF, in vitro fertilization; LD, live donor.

Figure 2 .
Figure 2. Flow diagram of study selection and data analysis strategies.H-index, Hirsh index; IRW, impact relative to the world; WOSCC, Web of Science Core Collection.

Figure 3 .
Figure 3. Baseline bibliometric characteristics of all eligible documents.(A) Pie chart showing the article types of the 425 papers.(B) Annual publications and citations, as well as (C) citation impact and citation per year about UTx.No data was produced in 1954 because the paper received no citation.(D) Document percent and citation impact according to the research areas of human UTx studies.

Figure 4 .
Figure 4. History and milestone of human UTx.Years and countries of most first events and encouraging achievements were shown.ART, assisted reproductive technology.

Figure 5 .
Figure 5. Relationship and cluster of countries.(A) Classification of countries according to the income levels.(B) Geographical UTx activity based on the number of publications.(C) The relationship between international and domestic collaborations.(D) Cooperative relationships among various countries.

Figure 6 .
Figure 6.Visualization of the institutions and authors.(A) Collaboration network of the top 40 institutions.(B) Network showing the authors' relationships.Each circle represents an author, and the different colors represent the years.

Figure 7 .
Figure 7. Participants of journals in human UTx.(A) Relationship of the representative journals.The number of links indicated the impact of scholarly publications.(B) Distributions of the open access types.

Figure 8 .
Figure 8. Analysis of keyword co-occurrence.(A) Clustering co-occurrence map of all keywords of studies on UTx.(B) Top 25 keywords with the strongest citation bursts.Matrix visualization (C) and mountain visualization (D) of bi-clustering of the key keywords.The row labels denote high-frequency keywords.The height of the mountain is proportional to the similarity within the cluster.

Figure 9 .
Figure 9. Human uterine graft with arterial and venous anastomoses.(A) Schematic picture of the vasculature network of the female reproductive tract.(B) Both uterine arteries are anastomosed to the recipient's external iliac arteries end-to-side.The recipient's uterine veins are anastomosed to the recipient's external iliac vein end-to-side.(C) The utero-ovarian veins are anastomosed end-to-side to a uterine vein.a. artery; v. vein.

Table 1
Indications for academic influence metrics in this study.
Leading scientific publisher Wiley published 6 of the top 14 journals, while Elsevier Science Inc. and Lippincott Williams & Wilkins accounted for 3 journals each.More than half of the journals (8/14) fell into the Q1 category, and three Q4 journals had corresponding low H-indexes.Remarkably, none of the journals published relevant papers before 2004.On the other hand, Fertility and Sterility has consistently demonstrated productivity in UTx since 2013, while all UTx papers published in Clinical Obstetrics and Gynecology were published in 2023.In addition, 50% of all journals were open access, with gold access accounting for 20% (Fig.7B).The presence of more OA (open access) papers could benefit the field by offering greater visibility and attracting more readers.Overall, these findings demonstrate that journals from various publishers, countries, quartile categories, and access choices actively participated in the research on UTx.

Table 2
Top 10productive countries in the uterus transplantation (UTx) field.

Table 3
Top 10 institutions ranked by the counts of publications.

Table 4
Top 10 most productive authors ranked by the numbers of publications.

Table 5
Top 10 cited original articles.

Table 6
Top journals ranked by the counts of publications.

Table 7
Top 20keywords with the highest frequency related to the human UTx through Citespace.