Multimodal ultrasound in evaluation of the endometrial receptivity in patients with different ultrasonic classifications of AM

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Methods A total of 100 patients diagnosed with AM were categorised into three subgroups: 26 with focal AM, 40 with diffuse AM, 34 with mixed AM. A control group comprised 44 healthy females. All participants underwent transvaginal ultrasound between the 10th and 14th day of their normal menstrual cycle.Measurements included endometrial thickness, uterine artery pulsatility index (PI), endometrial classification, blood perfusion, intima-muscular junction zone (JZ), direction of endometrial peristalsis, endometrial volume (EV), vascular index (VI), flow index (FI), and vascular blood flow index (VFI). A modified endometrial receptivity ultrasound scoring system was devised, and differences in these ultrasound indices and comprehensive endometrial receptivity scores across the four groups were analysed. Results Except for uterine artery PI, statistically significant differences were observed across the four groups in terms of intima thickness, EV, intima type, intima blood flow score, VI, FI, VFI, JZ, intima peristalsis, and comprehensive endometrial receptivity scores(all P ≤ 0.01). Comprehensive scores of endometrial receptivity were sequentially lower in the control group, focal AM group, diffuse AM group, mixed AM group, with each pairwise comparison being statistically significant ( P < 0.05). Conclusions Endometrial receptivity in patients with AM is compromised. The refined endometrial receptivity ultrasound scoring system offers a comprehensive assessment of endometrial receptivity in AM patients, the severity of endometrial receptivity impairment is most pronounced in patients with mixed AM, followed by diffuse AM, and least in focal AM. adenomyosis ultrasound endometrial receptivity score Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Introduction Adenomyosis (AM) is a prevalent condition characterized by the encroachment of endometrial glands and stroma into the myometrium, most frequently observed in women of reproductive age. Clinical manifestations include dysmenorrhoea, increased menstrual volume, pelvic pain, and infertility [ 1 ] . Recent studies have underscored that AM adversely affects not only the natural conception rates but also the clinical pregnancy and ongoing pregnancy rates in patients undergoing in vitro fertilization-embryo transfer (IVF-ET), with outcomes notably worse than those of women without AM. Particularly, severe AM significantly diminishes fertility [ 2 – 6 ] . An animal case-control study, after controlling for endometriosis, highlighted AM's strong association with primary infertility [ 7 ] . Younes [ 8 ] revealed in a meta-analysis that up to 30%–40% of infertility patients undergoing assisted reproductive technologies are affected by AM, establishing AM as a significant factor in female infertility. Embryo quality and endometrial receptivity emerge as critical determinants of transplant success, with the latter being implicated in two-thirds of infertility cases [ 9 ] . Endometrial receptivity, crucial for reproductive success, is negatively impacted by AM through mechanisms such as aberrant endometrial angiogenesis, a persistently hypoxic microenvironment, and compromised decidualization of endometrial stromal cells [ 10 – 12 ] , thus influencing pregnancy outcomes to a considerable extent [ 13 ] . Transvaginal ultrasound represents a common, economical, non-invasive, and efficacious modality for diagnosing AM and assessing endometrial receptivity. Based on sonographic characteristics, AM is categorized into focal, diffuse, and mixed types. However, there is an international scarcity of research on evaluating endometrial receptivity via transvaginal ultrasound in patients with different ultrasonic types of AM. Therefore, this study aims to explore the evaluative significance of various indices and an modified ultrasound scoring system for endometrial receptivity across the different ultrasonic manifestations of AM through transvaginal ultrasound examination. 1. Materials and method 1.1 Research object It was a prospective study. A total of 100 continuous cases of AM patients were randomly selected as the case group from January 2023 to February 2024, and continuous 44 healthy volunteers were randomly selected as the control group. All participants were duly informed about the study details and provided their written informed consent prior to inclusion. The study received approval from the Ethics Committee of the hospital (Ethics number [2023] No. 273). 1.2 Inclusion criteria and exclusion criteria Inclusion criteria: (1) Sexual life history; (2)Age ≥20 and ≤40 years old;(3) Normal uterine morphology; (4) Normal menstrual cycle on the 10th~14th day; (5) heart, liver, lung, kidney and other organ lesions; (6) All informed consent and voluntary participation. Exclusion criteria: (1) Suffering from other intrauterine diseases, such as submucosal fibroids, endometrial polyps, endometrial cavity fluid, uterine adhesions; (2) The ultrasound image quality is unclear; (3) Incomplete data collection and loss of follow-up. 1.3 Examination instruments Voluson E10 color Doppler ultrasonic diagnostic instrument of GE, equipped with 3D cavity content product probe, frequency is 5~9MHz. 1.4 Check Methods All participants were examined by a strictly trained sonographer and underwent transvaginal ultrasound between the 10th and 14th days of their normal menstrual cycle. Prior to the examination, patients were instructed to empty their bladders and took the lithotomy position. The ultrasound probe was disinfected with sanitizing wipes, lubricated with a coupling agent, covered with a protective condom, and gently introduced into the vaginal fornix of the examinee. Initially, a two-dimensional ultrasound was conducted on the median sagittal plane of the endometrium, with local magnification applied to assess the endometrial echo and morphology, and to classify the endometrium. Subsequently, the cursor was positioned at the thickest part of the endometrium to measure its thickness (Figure 1). Participants were requested to breathe steadily while the operator, holding the probe stationary, observed and recorded endometrial peristalsis for 2 minutes in a static state. The examination then proceeded to color Doppler mode to scan the median sagittal plane of the endometrium, observing endometrial blood flow under color Doppler ultrasound, and assigning scores based on predefined criteria (Figure 2). The bilateral uterine arteries were located at the level of the cervix's internal opening on both sides, and their pulsatility index (PI) was measured using Doppler ultrasound when at least three continuous, stable waveforms of uniform shape were acquired, with the average PI of both uterine arteries recorded as the result (Figure 3). The uterus was visualized on the median sagittal section using three-dimensional ultrasound imaging technology to assess the junctional zone (JZ) (Figure 4). Subsequently, the virtual organ computer-aided analysis (VOCAL) software was used, parameters were adjusted to preset values: sector scan angle 150°, color gain Gn 0.8, filter file low2, quality qual norm, pulse repetition rate 0.8kHz,, and the endometrial contour was manually delineated, with a 15° angle selected for each measurement and the contour drawn twelve times before finalization. This process yielded measurements of endometrial volume (EV), vascularization index (VI), flow index (FI), and vascular flow index (VFI) among other parameters (Figure 5). 1.5 Diagnostic criteria and evaluation criteria (1) AM Diagnosis: The diagnosis of adenomyosis (AM) was established in line with the clinical presentations of AM, such as menstrual irregularities, progressively worsening secondary dysmenorrhoea, infertility, among other clinical manifestations, and adhered to the ultrasonic diagnostic criteria set forth in the Morphological Uterus Sonographic Assessment (MUSA) consensus [14] . Following the diagnostic criteria from the Sonographic Classification and Reporting System of Adenomyosis (AM-SCRS) [15] , patients were categorized into focal AM group, diffuse AM group, and mixed AM group. (2) Evaluation criteria According to the Gonen classification criteria [16] , endometrial echoes were differentiated into three types: Type A, presenting a typical three-line sign; Type B, where a trilinear sign is vaguely visible, the endometrium exhibits a moderate intensity echo, and the high echo uterine line is intermittent and unclear; Type C, lacking a trilinear sign, displaying homogeneous hyperechoic endometrium, with the uterine line not discernible. In line with the International Endometrial Tumor Analysis (IETA) consensus [17] , the JZ appearance was classified into four categories: regular, irregular, unclear, and interrupted. According to the Applebaum rating scale [18] , endometrial and subendometrial blood flow were assessed and allocated into four levels: Level 0, where blood flow is confined to the myometrium encircling the endometrium, indicating an absence of blood flow signal within the endometrium; Level 1, where blood flow reaches the JZ; Level 2, where blood flow extends into the functional layer of the endometrium; Level 3, where blood vessels reach the uterine line. As per the Ijland classification system [19] , endometrial peristalsis was segregated into five patterns: the positive wave mode, where peristalsis originates from the cervix and progresses towards the fundus; the opposite wave mode, characterized by peristalsis initiating simultaneously from the cervix and fundus towards the uterine cavity; the random wave mode, featuring small, rhythmless peristalsis originating from various parts of the uterine cavity; the no motility wave mode, denoting an absence of endometrial peristalsis; and the negative wave mode, where peristalsis begins at the fundus of the uterus and moves towards the cervix. 1.6 Modified endometrial receptivity ultrasound scoring system The scoring system utilized in this investigation was developed in reference to the Applebaum rating scale [18] , and adapted to suit the specific conditions of this study(Table 1)). The maximum attainable score is 21 points, with higher scores indicative of enhanced endometrial receptivity. Table 1 Modified endometrial receptivity ultrasound scoring system 1.7 Statistical Methods All data were processed using SPSS27.0 statistical software. The counting data were represented by sample number (percentage), Chi-square test or Fisher exact probability method were used for data processing, and Bonferroni test was used to correct the significance level. Kolmogorov-Smirnov test was used for normality test first. If the measurement data met or approximated the normal distribution, the mean ± standard deviation( ±s ) was used, analysis of variance was used; if the measurement data did not meet the normal distribution, the median (interquartile distance) was used, and Kruskal-Wallis H test was used. P < 0.05 was statistically significant. Bland-Alterman test was used to determine the consistency of endometrial receptivity ultrasound scores among different physicians 2. Results 2.1 General Information This study comprised 44 participants in the control group and 100 patients diagnosed with AM, including 26 in the focal AM group, 40 in the diffuse AM group, and 34 in the mixed AM group. There was no statistically significant difference in age, BMI, number of pregnancies, number of births, and presence or absence of symptoms among the four groups (all P > 0.05) (Table 2) . 2.2 Comparison of endometrial thickness, EV and endometrial typing among the four groups Significant variations were observed in endometrial thickness and EV across the control, focal AM, diffuse AM, and mixed AM groups ( F =13.277 and 11.771, respectively, P <0.001). The endometrial thickness and EV were significantly lower in the mixed AM group than in the other three groups (P<0.05), and lower in the diffuse AM group than in the control group (all P0.05). Furthermore, substantial differences were noted in endometrial classification across the four groups ( χ 2 =38.844, P < 0.001). The proportion of Type A endometrium in the focal AM, diffuse AM, and mixed AM groups was significantly lower than in the control group, with a concomitant increase in Type C endometrium (all P 0.05) (Table 3). 2.3 Comparison of endometrial blood flow score, uterine artery PI value, VI, FI and VFI among the four groups Statistically significant differences in endometrial blood flow scores were evident among the control, focal AM, diffuse AM, and mixed AM groups ( χ 2 =34.727, P <0.001). The frequencies of endometrial blood flow scores of 0 and 1 were significantly higher in the diffuse AM and mixed AM groups compared with the control group, whereas the frequencies of scores 2 and 3 were significantly reduced ( P <0.05). There were no significant differences in endometrial blood flow scores between the control and focal AM groups, between the focal AM and diffuse AM groups, or between the focal AM and mixed AM groups, and between the diffuse AM and mixed AM groups (all P >0.05). Additionally, the VI, FI, and VFI demonstrated statistically significant variances across the four groups as a whole ( H =26.431, 15.948, and 29.428, respectively; P <0.001, 0.001, and <0.001). Notably, VI, FI, and VFI were significantly lower in the diffuse AM and mixed AM groups compared to the control group ( P <0.05), while no significant differences were observed in VI, FI, and VFI between the control and focal AM groups, between the focal AM and diffuse AM groups, between the focal AM and mixed AM groups, and between the diffuse AM and mixed AM groups ( P >0.05). The pulsatility index (PI) of uterine artery flow showed no significant variation among the four groups ( F =0.911, P =0.438) (Table 4). 2.4 Comparison of JZ, intima peristalsis direction and comprehensive endometrial receptivity scores among the four groups Significant disparities were observed in the JZ among the control group, focal AM group, diffuse AM group, and mixed AM group ( χ 2 =54.606, P <0.001). The frequency of regular JZ in the focal AM, diffuse AM, and mixed AM groups was considerably lower than in the control group (all P <0.05). Furthermore, the incidence of regular JZ in the mixed AM group was significantly reduced compared to both the focal and diffuse AM groups (all P <0.05). The occurrence of irregular and unclear JZ in the diffuse and mixed AM groups was markedly higher than in the control and focal AM groups (all P 0.05). Additionally, substantial differences were found in the direction of endometrial peristalsis across the control group, focal AM group, diffuse AM group, and mixed AM group collectively ( χ 2 =26.253, P =0.01). The prevalence of endometria exhibiting opposite wave mode in the diffuse AM and mixed AM groups was significantly less than in the control and focal AM groups ( P <0.05), and the proportion of endometria with no motility wave mode in the mixed AM group was significantly elevated compared to the other three groups ( P 0.05). Upon application of the modified endometrial receptivity ultrasound scoring system, it was discerned that the comprehensive endometrial receptivity scores in the three AM groups were significantly lower than those in the control group, demonstrating statistical significance (all P < 0.05). The scores of endometrial receptivity sequentially declined from the focal AM group to the diffuse AM group, and to the mixed AM group, with each pairwise comparison revealing statistical significance ( P <0.05) (Table 5). 3. Discussion Endometrial receptivity encapsulates the capacity of the endometrium to facilitate the blastocyst's localization, adhesion, invasion, and ultimately, the acceptance of embryo implantation within a specific temporal and spatial frame. Transvaginal ultrasound emerges as a prevalent method for evaluating endometrial receptivity, offering the benefits of being convenient, cost-effective, non-invasive, and capable of providing real-time data. Key ultrasound metrics commonly employed include endometrial thickness, classification, echo, JZ, direction of endometrial peristalsis, EV, uterine artery PI, endometrial blood flow score, VI, FI, and VFI [20, 21] . Nonetheless, a global consensus on the most precise ultrasound indicators for assessing endometrial receptivity and their optimal clinical application remains elusive. AM exhibits considerable heterogeneity. Research has indicated a correlation between the fertility of AM patients and the disease's classification [22] . Bourdon et al., in their study on the association between MRI categorization of AM and infertility, noted a reduced likelihood of infertility in patients with internal AM compared to those with external AM [5] . However, no uniform standard for AM classification exists in clinical practice. Histopathologically, AM is typically categorized into diffuse, nodular, sclerotic, and cystic types based on lesion infiltration depth, a system applicable solely to post-surgical patients and not to women of reproductive age [23] . Although MRI serves both for diagnosing and classifying AM, its drawbacks include lengthy procedure times and high costs, making it less accessible for financially constrained patients and potentially causing psychological distress. In 2019, Van dB et al. introduced a novel ultrasound classification for AM in the AM-SCRS [15] , delineating focal AM when over 25% of the lesion circumference is encased by normal myometrium, and diffuse AM otherwise. Lesions indistinguishable as either focal or diffuse are categorized as diffuse. Cases exhibiting both focal and diffuse characteristics are classified as mixed type. Clear demarcation of lesions fully encircled by proliferative primary tissue is termed uterine adenomyoma and classified under focal AM. This classification system, by virtue of its simplicity and practicality, provides an accurate and intuitive assessment of the lesion in relation to surrounding normal myometrium, thereby holding significant clinical relevance. The findings of this study illustrate that the indicators of endometrial receptivity impairment, as well as the extent of this impairment, vary across different ultrasonic classifications of AM. Endometrial thickness, EV, and endometrial classification emerge as pivotal factors in the assessment of endometrial receptivity. It was observed that the likelihood of pregnancy was higher with an endometrial thickness ranging from 8 to 14mm compared to thicknesses under 8mm, a difference that was statistically significant [24] . Research conducted by Zhao et al. on 1933 patients undergoing IVF-ET identified an endometrial thickness threshold of 7mm, below which the probability of pregnancy significantly declined [25] . These findings underscore the importance of endometrial thickness as a determinant of the quality of endometrial receptivity, suggesting that receptivity is markedly enhanced at thicknesses of 8 to 14 mm and substantially diminished when thickness falls below 7 mm. In this study, the mean endometrial thickness in the focal AM group was not significantly different from that in the control group, whereas the mean thicknesses in the diffuse and mixed AM groups were notably lower than in the control group. Specifically, the average thickness in the diffuse AM group was less than 8mm, representing a statistically significant reduction compared to the control group. The mean thickness in the mixed AM group was 6.1mm, not only lower than that of the control group but also significantly reduced compared to the other two AM groups, indicating that different ultrasonic types of AM exert varying effects on endometrial thickness. Focal AM had minimal impact on thickness, while diffuse and mixed AM were associated with significant thinning of the endometrium, particularly pronounced in mixed AM. This variation may be attributed to the size and location of lesions: focal AM lesions are typically located in the outer myometrium and exert minimal influence on the endometrium, while diffuse or mixed AM lesions, being closer to the endometrium, potentially have a more significant impact. Moreover, mixed AM is often accompanied by substantial adenomyoma, leading to severe uterine deformation and pronounced endometrial thinning [22] . Both endometrial thickness and EV reflect the general dimensions of the uterine cavity, with endometrial thickness also indicative of EV to a degree. The patterns of EV variation and inter-group differences observed in this study paralleled those of endometrial thickness, suggesting that the impact of different ultrasonic types of AM on endometrial thickness is akin to their effect on EV. Furthermore, the study demonstrated a significant reduction in the proportion of type A endometrium and an increase in type C endometrium in the AM groups compared to the control group, with no significant differences in endometrial classification within the AM groups. Endometrial classification is reflective of the pre-implantation uterine environment, types B and C suggest a premature closure of the "embryo implantation window," unfavorable for subsequent embryo implantation [27] . Therefore, we think that AM disrupts the synchrony between the endometrium and the embryo by affecting the "embryo implantation window", thereby impacting endometrial receptivity. Additionally, some researchers propose that alterations in endometrial classification are closely linked to hormonal levels [28] , with disturbances in estrogen and progesterone levels among AM patients contributing to changes in endometrial classification. Endometrial and myometrial blood flow are commonly employed ultrasound parameters for evaluating endometrial receptivity. The endometrial blood flow score facilitates a semi-quantitative assessment of endometrial perfusion. VI, FI, and VFI represent advanced observational metrics introduced with technological advancements in ultrasound, offering quantitative evaluation of endometrial perfusion with enhanced precision and significant clinical relevance. This study's findings revealed that within the case group, the occurrence of diffuse and mixed AM with endometrial blood flow scores of 3 and 2 was markedly lower compared to the control group, while scores of 0 and 1 were significantly more frequent, and VI, FI, and VFI values were also considerably reduced in comparison with the control group. Conversely, focal AM exhibited no significant differences from the control group in both semi-quantitative and quantitative measures of endometrial blood flow. This indicates that diffuse and mixed AM significantly impair endometrial blood perfusion, corroborating the findings of Vlahos et al. [29] . Focal AM, however, exerts minimal impact on endometrial perfusion. Furthermore, no statistical significance was observed between diffuse and mixed AM in the aforementioned blood flow ultrasound evaluation metrics, suggesting that the effects of diffuse and mixed AM on endometrial perfusion are coincident. This similarity in impact could be attributed to the adenomyotic lesions within AM and the consequent compression of blood vessels, leading to diminished endometrial blood supply. In contrast, focal AM, due to its limited contact with the endometrium, has negligible influence on blood flow. In the evaluation of ultrasound indicators for the JZ and endometrial peristalsis, it was observed that the incidence of regular JZ appearances in the focal, diffuse, and mixed AM groups was significantly lower than in the control group, suggesting that AM contributes to the deterioration of JZ morphology in patients. Additionally, the study noted an elevated frequency of irregular and unclear JZ in the mixed and diffuse types compared with the focal type, while the occurrence of regular JZ in the mixed type was significantly diminished relative to both focal and diffuse types. This indicates a variability in the extent of JZ impairment across different ultrasonic classifications of AM, with a progressive increase in damage from focal to diffuse and mixed types. Rasmussen et al. have similarly highlighted that the JZ in AM patients is compromised [30] , aligning with the outcomes of this investigation, though their research did not differentiate between AM based on ultrasonic typology. The alteration in JZ is associated with the levels of ovarian hormones in patients, leading to the hypothesis that the varying degrees of JZ impairment in different ultrasonic types of AM may be linked to hormonal levels. This study also determined significant differences in endometrial motion between the diffuse and mixed AM groups compared to the control and focal AM groups, whereas endometrial peristalsis in focal AM was not significantly divergent from that in the control group. The consensus among many researchers is that changes in endometrial peristalsis are attributable to abnormal JZ morphology [31] . In patients with AM, compromised JZ integrity results in altered endometrial peristalsis. Our findings suggest that focal AM-associated JZ morphology lesions do not markedly affect endometrial peristalsis, implying that alterations in JZ do not invariably lead to peristalsis abnormalities, potentially due to the extent of JZ damage. Recent studies indicate that AM may induce increased myometrial stiffness [32] , and abnormal myometrial stiffness could alter myometrial layer peristalsis, thereby influencing endometrial peristalsis. The specific impact of AM on endometrial peristalsis remains to be fully elucidated, necessitating further investigation. Notably, this study found no significant differences in uterine artery PI values among the four groups, suggesting that AM might not affect uterine arterial blood flow in patients. Contrarily, some researches show that AM could elevate PI values by increasing uterine arterial blood flow [33] . Given reports of uterine artery blood flow parameters varying across menstrual cycles [34] , it is considered that these findings may relate to the timing of the study, warranting additional research for validation. Ultrasound serves not only as a prevalent diagnostic tool for AM but also as a means to assess endometrial receptivity. Currently, investigations into the endometrial receptivity of AM categorized by different ultrasonic types are limited. Earlier studies focusing on the ultrasound evaluation of endometrial receptivity often relied on a solitary indicator. Recent research findings suggest that the precision of using a single parameter to evaluate endometrial receptivity falls short compared to an association of multiple indicators, offering a more holistic assessment of the endometrial state and furnishing clinicians with more reliable diagnostic data [35] . The endometrial receptivity ultrasound scoring system facilitates the association of numerous indicators, quantifying subjective assessments to yield more objective and comprehensive outcomes, thereby establishing itself as a dependable evaluation technique. The scoring system employed in this investigation, refined from the Applebaum scoring method and integrated with findings from previous studies, aligns more closely with clinical practice and is logically sound. Utilizing an modified endometrial receptivity ultrasound scoring system, this study assigned scores to patients with various ultrasonic types of AM. The outcomes indicated that the control group achieved the highest overall score, with the mixed AM group registering the lowest comprehensive score, followed by the diffuse and focal types, respectively, with each pairwise comparison reaching statistical significance. This underscores that AM impairs endometrial receptivity, with varying degrees of receptivity damage across different ultrasonic classifications of AM, and a progressive increase in damage severity from focal to diffuse and mixed AM. Scholars have previously noted that the endometrial receptivity in diffuse AM is inferior to that in focal AM [36, 37] , aligning with the findings of this study. However, given the categorization differences, prior research on AM's impact on endometrial receptivity predominantly covered the focal and diffuse types, with no studies specifically addressing the ultrasound evaluation of endometrial receptivity in mixed AM. Mixed AM, embodying both focal and diffuse traits, typically manifests in advanced stages of the condition, which may elucidate the most pronounced impact on endometrial receptivity observed in mixed AM. In conclusion, adenomyosis compromises endometrial receptivity through alterations in endometrial morphology, thickness, classification, intimal blood flow index, JZ, endometrial peristalsis, among other factors. The indices of endometrial receptivity impairment and the extent of damage vary across different ultrasonic classifications of adenomyosis. The endometrial receptivity ultrasound scoring system addresses the limitations of relying on a single ultrasound parameter and presents an effective method for assessing endometrial receptivity. Analysis using the modified endometrial receptivity ultrasound scoring system for various ultrasonic types of adenomyosis revealed that the endometrial receptivity in cases of mixed adenomyosis was significantly inferior compared to the other two types, with the receptivity in diffuse adenomyosis being lower than in focal adenomyosis. Thus, it is advisable to perform comprehensive transvaginal ultrasound examinations and ultrasonic classifications for adenomyosis patients contemplating pregnancy. Should the ultrasound suggest mixed adenomyosis, clinicians are urged to undertake interventions to enhance the probability of successful pregnancy outcomes. 4. Conclusion The receptivity of the endometrium in patients with AM is diminished. The ultrasonic indices of endometrial receptivity impairment and the degree of damage vary among different ultrasonic types of AM, with mixed and diffuse AM showing particularly significant differences. Using the modified endometrial receptivity ultrasound scoring system to evaluate the endometrial receptivity of AM patients shows that the greatest reduction in endometrial receptivity is observed in patients with mixed AM, succeeded by those with diffuse AM, and least in those with focal AM. Declarations Acknowledgements Not applicable. Authors' contributions Kailing Tan：Conceptualization, Data curation, Writing–original draft Yifang Ye：Formal analysis, Investigation, Writing – original draft Jiemin Chen、Yaqian Zhang：Software, Resources, Writing – review & editing Qiuyue Chen: Methodology, Project administration, Writing – review & editing Guorong Lyu: Supervision, Validation, Visualization, Writing – review & editing Funding Statement: This study was supported by the Fujian Provincial Department of Science and Technology (NO. 2019J01478). Data Availability The raw data supporting the conclusions of this article will be made available by the authors on request. Ethics approval and consent to participate The study was approved by the Ethics Committee of the Second Affiliated Hospital of Fujian Medical University (NO. 2023-272), All participants were informed about the study protocol and provided written informed consent to participate in the study. 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Impact of letrozole versus clomiphene citrate on endometrial receptivity in Iraqi women with polycystic ovarian syndrome[J]. J Clin Pharm Ther, 2019,44:618-22. Vlahos NF, Theodoridis TD, Partsinevelos GA. Myomas and adenomyosis: impact on reproductive outcome[J]. Biomed Res Int, 2017,2017:5926470. Rasmussen CK, Hansen ES, Dueholm M. Two-and three-dimensional ultrasonographic features related to histopathology of the uterine endometrial-myometrial junctional zone[J]. Acta Obstet Gynecol Scand, 2019,98:205-14. Tanos V, Lingwood L, Balami S. Junctional zone endometrium morphological characteristics and functionality: review of the literature[J]. Gynecol Obstet Invest, 2020,85:107-17. Brunelli AC, Brito LGO, Moro FAS, Jales RM, Yela DA, Benetti-Pinto CL. Ultrasound Elastography for the Diagnosis of Endometriosis and Adenomyosis: A Systematic Review with Meta-analysis[J]. Ultrasound Med Biol, 2023,49:699-709. Jeng CJ, Ou KY, Long CY, Chuang L, Ker CR. 500 cases of high-intensity focused ultrasound (HIFU) ablated uterine fibroids and adenomyosis[J]. Taiwan J Obstet Gynecol, 2020,59:865-71. Dogan O, Yildiz A, Temizkan O, Pulatoglu C. Comparison of uterine, endometrial and ovarian blood flow by transvaginal color doppler ultrasound in ovulatory and anovulatory cycles[J]. Ginekol Pol, 2016,87:581-4. Wang Xiaoxuan. Evaluation of endometrial receptivity in patients with freeze-thaw embryo transfer by ultrasonic multimodal scores [D]. Shandong University. 2023. Tamura H, Kishi H, Kitade M, Asai-Sato M, Tanaka A, Murakami T, et al. Complications and outcomes of pregnant women with adenomyosis in Japan[J]. Reprod Med Biol, 2017,16:330-6. Tamura H, Kishi H, Kitade M, Asai-Sato M, Tanaka A, Murakami T, et al. Clinical outcomes of infertility treatment for women with adenomyosis in Japan[J]. Reprod Med Biol, 2017,16:276-82. Tables Tables 1 to 5 are available in the Supplementary Files section. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-8194490","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":556850669,"identity":"cd02abe4-d7b1-4b60-a627-d16e5606d31f","order_by":0,"name":"Kailing Tan","email":"","orcid":"","institution":"The Second Affiliated Hospital of Fujian Medical University","correspondingAuthor":false,"prefix":"","firstName":"Kailing","middleName":"","lastName":"Tan","suffix":""},{"id":556850670,"identity":"fddfaad4-603c-4e92-9f65-bd44ddfbd8f6","order_by":1,"name":"Yifang Ye","email":"","orcid":"","institution":"The Second Affiliated Hospital of Fujian 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1","display":"","copyAsset":false,"role":"figure","size":611952,"visible":true,"origin":"","legend":"\u003cp\u003eMeasurement of endometrial thickness\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-8194490/v1/c673b8cb97ba21a27763a8c1.png"},{"id":98421835,"identity":"88f70a90-e4ca-41ef-9f87-0c524b86093f","added_by":"auto","created_at":"2025-12-17 16:29:35","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":742508,"visible":true,"origin":"","legend":"\u003cp\u003eEndometrial blood flow score\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-8194490/v1/00eb3a71b5268dad1c752750.png"},{"id":97932106,"identity":"30b7c3a7-6893-45b2-8279-b3a6f11a0dab","added_by":"auto","created_at":"2025-12-11 00:43:03","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":673008,"visible":true,"origin":"","legend":"\u003cp\u003eMeasurement of uterine arterial blood flow\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-8194490/v1/55264f4a40d98646fd518d26.png"},{"id":98421660,"identity":"024b0fb3-4518-4b02-8d23-f52d77ae108a","added_by":"auto","created_at":"2025-12-17 16:28:51","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":751097,"visible":true,"origin":"","legend":"\u003cp\u003eThree-dimensional imaging of uterus for evaluation of JZ\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-8194490/v1/4433964b1db088c13cb51ab9.png"},{"id":97932113,"identity":"76141def-ae42-46aa-abb0-8783d3a03beb","added_by":"auto","created_at":"2025-12-11 00:43:03","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":540013,"visible":true,"origin":"","legend":"\u003cp\u003eVOCAL technology detects EV, VI, FI and VFI\u003c/p\u003e","description":"","filename":"5.png","url":"https://assets-eu.researchsquare.com/files/rs-8194490/v1/26f31849b781fb83d8fabbf8.png"},{"id":107977946,"identity":"650924c8-ce2b-4981-bedc-54ee92c54f8f","added_by":"auto","created_at":"2026-04-28 07:55:56","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":5267482,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-8194490/v1/84215ef7-286d-4f33-9f42-583b43a3c5cd.pdf"},{"id":97932099,"identity":"d46c1e36-8c30-4ca0-810f-23dbe8b7e444","added_by":"auto","created_at":"2025-12-11 00:43:03","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":35244,"visible":true,"origin":"","legend":"","description":"","filename":"Tables.docx","url":"https://assets-eu.researchsquare.com/files/rs-8194490/v1/e33eef887380b23b5690aea6.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Multimodal ultrasound in evaluation of the endometrial receptivity in patients with different ultrasonic classifications of AM","fulltext":[{"header":"Introduction","content":"\u003cp\u003eAdenomyosis (AM) is a prevalent condition characterized by the encroachment of endometrial glands and stroma into the myometrium, most frequently observed in women of reproductive age. Clinical manifestations include dysmenorrhoea, increased menstrual volume, pelvic pain, and infertility\u003csup\u003e[\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]\u003c/sup\u003e. Recent studies have underscored that AM adversely affects not only the natural conception rates but also the clinical pregnancy and ongoing pregnancy rates in patients undergoing in vitro fertilization-embryo transfer (IVF-ET), with outcomes notably worse than those of women without AM. Particularly, severe AM significantly diminishes fertility\u003csup\u003e[\u003cspan additionalcitationids=\"CR3 CR4 CR5\" citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e]\u003c/sup\u003e. An animal case-control study, after controlling for endometriosis, highlighted AM's strong association with primary infertility\u003csup\u003e[\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e]\u003c/sup\u003e. Younes\u003csup\u003e[\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]\u003c/sup\u003e revealed in a meta-analysis that up to 30%\u0026ndash;40% of infertility patients undergoing assisted reproductive technologies are affected by AM, establishing AM as a significant factor in female infertility. Embryo quality and endometrial receptivity emerge as critical determinants of transplant success, with the latter being implicated in two-thirds of infertility cases\u003csup\u003e[\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e]\u003c/sup\u003e. Endometrial receptivity, crucial for reproductive success, is negatively impacted by AM through mechanisms such as aberrant endometrial angiogenesis, a persistently hypoxic microenvironment, and compromised decidualization of endometrial stromal cells\u003csup\u003e[\u003cspan additionalcitationids=\"CR11\" citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e]\u003c/sup\u003e, thus influencing pregnancy outcomes to a considerable extent\u003csup\u003e[\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e]\u003c/sup\u003e. Transvaginal ultrasound represents a common, economical, non-invasive, and efficacious modality for diagnosing AM and assessing endometrial receptivity. Based on sonographic characteristics, AM is categorized into focal, diffuse, and mixed types. However, there is an international scarcity of research on evaluating endometrial receptivity via transvaginal ultrasound in patients with different ultrasonic types of AM. Therefore, this study aims to explore the evaluative significance of various indices and an modified ultrasound scoring system for endometrial receptivity across the different ultrasonic manifestations of AM through transvaginal ultrasound examination.\u003c/p\u003e"},{"header":"1. Materials and method","content":"\u003cp\u003e1.1 Research object\u003c/p\u003e\n\u003cp\u003eIt was a prospective study. A total of 100 continuous cases of AM patients were randomly selected as the case group from January 2023 to February 2024, and continuous 44 healthy volunteers were randomly selected as the control group. All participants were duly informed about the study details and provided their written informed consent prior to inclusion. The study received approval from the Ethics Committee of the hospital (Ethics number [2023] No. 273).\u003c/p\u003e\n\u003cp\u003e1.2 Inclusion criteria and exclusion criteria\u003c/p\u003e\n\u003cp\u003eInclusion criteria: (1) Sexual life history; (2)Age \u0026ge;20 and \u0026le;40 years old;(3) Normal uterine morphology; (4) Normal menstrual cycle on the 10th~14th day; (5) heart, liver, lung, kidney and other organ lesions; (6) All informed consent and voluntary participation.\u003c/p\u003e\n\u003cp\u003eExclusion criteria: (1) Suffering from other intrauterine diseases, such as submucosal fibroids, endometrial polyps, endometrial cavity fluid, uterine adhesions; (2) The ultrasound image quality is unclear; (3) Incomplete data collection and loss of follow-up. \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp;\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e1.3 Examination instruments\u003c/p\u003e\n\u003cp\u003eVoluson E10 color Doppler ultrasonic diagnostic instrument of GE, equipped with 3D cavity content product probe, frequency is 5~9MHz.\u003c/p\u003e\n\u003cp\u003e1.4 Check Methods\u003c/p\u003e\n\u003cp\u003eAll participants were examined by a strictly trained sonographer and underwent transvaginal ultrasound between the 10th and 14th days of their normal menstrual cycle. Prior to the examination, patients were instructed to empty their bladders and took the lithotomy position. The ultrasound probe was disinfected with sanitizing wipes, lubricated with a coupling agent, covered with a protective condom, and gently introduced into the vaginal fornix of the examinee. Initially, a two-dimensional ultrasound was conducted on the median sagittal plane of the endometrium, with local magnification applied to assess the endometrial echo and morphology, and to classify the endometrium. Subsequently, the cursor was positioned at the thickest part of the endometrium to measure its thickness (Figure 1). Participants were requested to breathe steadily while the operator, holding the probe stationary, observed and recorded endometrial peristalsis for 2 minutes in a static state. The examination then proceeded to color Doppler mode to scan the median sagittal plane of the endometrium, observing endometrial blood flow under color Doppler ultrasound, and assigning scores based on predefined criteria (Figure 2). The bilateral uterine arteries were located at the level of the cervix\u0026apos;s internal opening on both sides, and their pulsatility index (PI) was measured using Doppler ultrasound when at least three continuous, stable waveforms of uniform shape were acquired, with the average PI of both uterine arteries recorded as the result (Figure 3). The uterus was visualized on the median sagittal section using three-dimensional ultrasound imaging technology to assess the junctional zone (JZ) (Figure 4). Subsequently, the virtual organ computer-aided analysis (VOCAL) software was used, parameters were adjusted to preset values: sector scan angle 150\u0026deg;, color gain Gn 0.8, filter file low2, quality qual norm, pulse repetition rate 0.8kHz,, and the endometrial contour was manually delineated, with a 15\u0026deg; angle selected for each measurement and the contour drawn twelve times before finalization. This process yielded measurements of endometrial volume (EV), vascularization index (VI), flow index (FI), and vascular flow index (VFI) among other parameters (Figure 5).\u003c/p\u003e\n\u003cp\u003e1.5 Diagnostic criteria and evaluation criteria\u003c/p\u003e\n\u003cp\u003e(1) AM Diagnosis: The diagnosis of adenomyosis (AM) was established in line with the clinical presentations of AM, such as menstrual irregularities, progressively worsening secondary dysmenorrhoea, infertility, among other clinical manifestations, and adhered to the ultrasonic diagnostic criteria set forth in the Morphological Uterus Sonographic Assessment (MUSA) consensus\u003csup\u003e[14]\u003c/sup\u003e. Following the diagnostic criteria from the Sonographic Classification and Reporting System of Adenomyosis (AM-SCRS)\u003csup\u003e[15]\u003c/sup\u003e, patients were categorized into focal AM group, diffuse AM group, and mixed AM group.\u003c/p\u003e\n\u003cp\u003e(2) Evaluation criteria\u003c/p\u003e\n\u003cp\u003eAccording to the Gonen classification criteria \u003csup\u003e[16]\u003c/sup\u003e, endometrial echoes were differentiated into three types: Type A, presenting a typical three-line sign; Type B, where a trilinear sign is vaguely visible, the endometrium exhibits a moderate intensity echo, and the high echo uterine line is intermittent and unclear; Type C, lacking a trilinear sign, displaying homogeneous hyperechoic endometrium, with the uterine line not discernible.\u003c/p\u003e\n\u003cp\u003eIn line with the International Endometrial Tumor Analysis (IETA) consensus\u003csup\u003e[17]\u003c/sup\u003e, the JZ appearance was classified into four categories: regular, irregular, unclear, and interrupted.\u003c/p\u003e\n\u003cp\u003eAccording to the Applebaum rating scale \u003csup\u003e[18]\u003c/sup\u003e, endometrial and subendometrial blood flow were assessed and allocated into four levels: Level 0, where blood flow is confined to the myometrium encircling the endometrium, indicating an absence of blood flow signal within the endometrium; Level 1, where blood flow reaches the JZ; Level 2, where blood flow extends into the functional layer of the endometrium; Level 3, where blood vessels reach the uterine line.\u003c/p\u003e\n\u003cp\u003eAs per the Ijland classification system\u003csup\u003e[19]\u003c/sup\u003e, endometrial peristalsis was segregated into five patterns: the positive wave mode, where peristalsis originates from the cervix and progresses towards the fundus; the opposite wave mode, characterized by peristalsis initiating simultaneously from the cervix and fundus towards the uterine cavity; the random wave mode, featuring small, rhythmless peristalsis originating from various parts of the uterine cavity; the no motility wave mode, denoting an absence of endometrial peristalsis; and the negative wave mode, where peristalsis begins at the fundus of the uterus and moves towards the cervix.\u003c/p\u003e\n\u003cp\u003e1.6 Modified endometrial receptivity ultrasound scoring system\u003c/p\u003e\n\u003cp\u003eThe scoring system utilized in this investigation was developed in reference to the Applebaum rating scale\u003csup\u003e[18]\u003c/sup\u003e, and adapted to suit the specific conditions of this study(Table 1)). The maximum attainable score is 21 points, with higher scores indicative of enhanced endometrial receptivity.\u003c/p\u003e\n\u003cp\u003eTable 1 Modified endometrial receptivity ultrasound scoring system\u003c/p\u003e\n\u003cp\u003e1.7 Statistical Methods\u003c/p\u003e\n\u003cp\u003eAll data were processed using SPSS27.0 statistical software. The counting data were represented by sample number (percentage), \u003cem\u003eChi-square\u003c/em\u003e test or \u003cem\u003eFisher\u003c/em\u003e exact probability method were used for data processing, and Bonferroni test was used to correct the significance level. \u003cem\u003eKolmogorov-Smirnov\u003c/em\u003e test was used for normality test first. If the measurement data met or approximated the normal distribution, the mean \u0026plusmn; standard deviation(\u003cimg width=\"11\" height=\"22\" src=\"https://myfiles.space/user_files/58895_8739fc6c57c1c19a/58895_custom_files/img1765375604.gif\" alt=\"image\"\u003e\u003cem\u003e\u0026plusmn;s\u003c/em\u003e) was used, analysis of variance was used; if the measurement data did not meet the normal distribution, the median (interquartile distance) was used, and \u003cem\u003eKruskal-Wallis H\u003c/em\u003e test was used. \u003cem\u003eP\u003c/em\u003e \u0026lt; 0.05 was statistically significant. Bland-Alterman test was used to determine the consistency of endometrial receptivity ultrasound scores among different physicians\u003c/p\u003e"},{"header":"2. Results","content":"\u003cp\u003e2.1 General Information\u003c/p\u003e\n\u003cp\u003eThis study comprised 44 participants in the control group and 100 patients diagnosed with AM, including 26 in the focal AM group, 40 in the diffuse AM group, and 34 in the mixed AM group. There was no statistically significant difference in age, BMI, number of pregnancies, number of births, and presence or absence of symptoms among the four groups (all \u003cem\u003eP\u003c/em\u003e \u0026gt; 0.05) (Table 2) .\u003c/p\u003e\n\u003cp\u003e2.2 Comparison of endometrial thickness, EV and endometrial typing among the four groups\u003c/p\u003e\n\u003cp\u003eSignificant variations were observed in endometrial thickness and EV across the control, focal AM, diffuse AM, and mixed AM groups (\u003cem\u003eF\u003c/em\u003e=13.277 and 11.771, respectively, \u003cem\u003eP\u003c/em\u003e\u0026lt;0.001). The endometrial thickness and EV were significantly lower in the mixed AM group than in the other three groups (P\u0026lt;0.05), and lower in the diffuse AM group than in the control group (all P\u0026lt;0.05). No significant differences in endometrial thickness and EV were observed between the control and focal AM groups, or between the focal and diffuse AM groups (all P\u0026gt;0.05). Furthermore, substantial differences were noted in endometrial classification across the four groups (\u003cem\u003e\u0026chi;\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e=38.844, \u003cem\u003eP\u003c/em\u003e\u0026lt; 0.001). The proportion of Type A endometrium in the focal AM, diffuse AM, and mixed AM groups was significantly lower than in the control group, with a concomitant increase in Type C endometrium (all \u003cem\u003eP\u003c/em\u003e\u0026lt;0.05). No significant differences were noted in endometrial classification within the AM groups (all \u003cem\u003eP\u003c/em\u003e\u0026gt;0.05) (Table 3).\u003c/p\u003e\n\u003cp\u003e2.3 Comparison of endometrial blood flow score, uterine artery PI value, VI, FI and VFI among the four groups\u003c/p\u003e\n\u003cp\u003eStatistically significant differences in endometrial blood flow scores were evident among the control, focal AM, diffuse AM, and mixed AM groups (\u003cem\u003e\u0026chi;\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e=34.727, \u003cem\u003eP\u003c/em\u003e\u0026lt;0.001). The frequencies of endometrial blood flow scores of 0 and 1 were significantly higher in the diffuse AM and mixed AM groups compared with the control group, whereas the frequencies of scores 2 and 3 were significantly reduced (\u003cem\u003eP\u003c/em\u003e\u0026lt;0.05). There were no significant differences in endometrial blood flow scores between the control and focal AM groups, between the focal AM and diffuse AM groups, or between the focal AM and mixed AM groups, and between the diffuse AM and mixed AM groups (all \u003cem\u003eP\u003c/em\u003e\u0026gt;0.05). Additionally, the VI, FI, and VFI demonstrated statistically significant variances across the four groups as a whole (\u003cem\u003eH\u003c/em\u003e=26.431, 15.948, and 29.428, respectively; \u003cem\u003eP\u003c/em\u003e\u0026lt;0.001, 0.001, and \u0026lt;0.001). Notably, VI, FI, and VFI were significantly lower in the diffuse AM and mixed AM groups compared to the control group (\u003cem\u003eP\u003c/em\u003e\u0026lt;0.05), while no significant differences were observed in VI, FI, and VFI between the control and focal AM groups, between the focal AM and diffuse AM groups, between the focal AM and mixed AM groups, and between the diffuse AM and mixed AM groups (\u003cem\u003eP\u003c/em\u003e\u0026gt;0.05). The pulsatility index (PI) of uterine artery flow showed no significant variation among the four groups (\u003cem\u003eF\u003c/em\u003e=0.911, \u003cem\u003eP\u003c/em\u003e=0.438) (Table 4).\u003c/p\u003e\n\u003cp\u003e2.4 Comparison of JZ, intima peristalsis direction and comprehensive endometrial receptivity scores\u0026nbsp;among the four groups\u003c/p\u003e\n\u003cp\u003eSignificant disparities were observed in the JZ among the control group, focal AM group, diffuse AM group, and mixed AM group (\u003cem\u003e\u0026chi;\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e=54.606,\u003cem\u003e\u0026nbsp;P\u003c/em\u003e\u0026lt;0.001). The frequency of regular JZ in the focal AM, diffuse AM, and mixed AM groups was considerably lower than in the control group (all \u003cem\u003eP\u003c/em\u003e\u0026lt;0.05). Furthermore, the incidence of regular JZ in the mixed AM group was significantly reduced compared to both the focal and diffuse AM groups (all\u003cem\u003e\u0026nbsp;P\u003c/em\u003e\u0026lt;0.05). The occurrence of irregular and unclear JZ in the diffuse and mixed AM groups was markedly higher than in the control and focal AM groups (all \u003cem\u003eP\u003c/em\u003e\u0026lt;0.05). No significant variation was noted in the interruption of JZ across the four groups (\u003cem\u003eP\u003c/em\u003e\u0026gt;0.05). Additionally, substantial differences were found in the direction of endometrial peristalsis across the control group, focal AM group, diffuse AM group, and mixed AM group collectively (\u003cem\u003e\u0026chi;\u003c/em\u003e\u003csup\u003e2\u003c/sup\u003e=26.253, \u003cem\u003eP\u003c/em\u003e=0.01). The prevalence of endometria exhibiting opposite wave mode in the diffuse AM and mixed AM groups was significantly less than in the control and focal AM groups (\u003cem\u003eP\u003c/em\u003e\u0026lt;0.05), and the proportion of endometria with no motility wave mode in the mixed AM group was significantly elevated compared to the other three groups (\u003cem\u003eP\u003c/em\u003e\u0026lt;0.05). There was no significant discrepancy in the positive wave mode, random wave mode, and negative wave mode among the four groups (\u003cem\u003eP\u003c/em\u003e\u0026gt;0.05). Upon application of the\u0026nbsp;modified endometrial receptivity ultrasound scoring system, it was discerned that the comprehensive endometrial receptivity scores in the three AM groups were significantly lower than those in the control group, demonstrating statistical significance (all \u003cem\u003eP\u003c/em\u003e\u0026lt; 0.05). The scores of endometrial receptivity sequentially declined from the focal AM group to the diffuse AM group, and to the mixed AM group, with each pairwise comparison revealing statistical significance (\u003cem\u003eP\u003c/em\u003e\u0026lt;0.05) (Table 5).\u003c/p\u003e"},{"header":"3. Discussion","content":"\u003cp\u003eEndometrial receptivity encapsulates the capacity of the endometrium to facilitate the blastocyst\u0026apos;s localization, adhesion, invasion, and ultimately, the acceptance of embryo implantation within a specific temporal and spatial frame. Transvaginal ultrasound emerges as a prevalent method for evaluating endometrial receptivity, offering the benefits of being convenient, cost-effective, non-invasive, and capable of providing real-time data. Key ultrasound metrics commonly employed include endometrial thickness, classification, echo, JZ, direction of endometrial peristalsis, EV, uterine artery PI, endometrial blood flow score, VI, FI, and VFI\u003csup\u003e[20, 21]\u003c/sup\u003e. Nonetheless, a global consensus on the most precise ultrasound indicators for assessing endometrial receptivity and their optimal clinical application remains elusive.\u003c/p\u003e\n\u003cp\u003eAM exhibits considerable heterogeneity. Research has indicated a correlation between the fertility of AM patients and the disease\u0026apos;s classification\u003csup\u003e[22]\u003c/sup\u003e. Bourdon et al., in their study on the association between MRI categorization of AM and infertility, noted a reduced likelihood of infertility in patients with internal AM compared to those with external AM\u003csup\u003e[5]\u003c/sup\u003e. However, no uniform standard for AM classification exists in clinical practice. Histopathologically, AM is typically categorized into diffuse, nodular, sclerotic, and cystic types based on lesion infiltration depth, a system applicable solely to post-surgical patients and not to women of reproductive age\u003csup\u003e[23]\u003c/sup\u003e. Although MRI serves both for diagnosing and classifying AM, its drawbacks include lengthy procedure times and high costs, making it less accessible for financially constrained patients and potentially causing psychological distress. In 2019, Van dB et al. introduced a novel ultrasound classification for AM in the AM-SCRS\u003csup\u003e[15]\u003c/sup\u003e, delineating focal AM when over 25% of the lesion circumference is encased by normal myometrium, and diffuse AM otherwise. Lesions indistinguishable as either focal or diffuse are categorized as diffuse. Cases exhibiting both focal and diffuse characteristics are classified as mixed type. Clear demarcation of lesions fully encircled by proliferative primary tissue is termed uterine adenomyoma and classified under focal AM. This classification system, by virtue of its simplicity and practicality, provides an accurate and intuitive assessment of the lesion in relation to surrounding normal myometrium, thereby holding significant clinical relevance.\u003c/p\u003e\n\u003cp\u003eThe findings of this study illustrate that the indicators of endometrial receptivity impairment, as well as the extent of this impairment, vary across different ultrasonic classifications of AM. Endometrial thickness, EV, and endometrial classification emerge as pivotal factors in the assessment of endometrial receptivity. It was observed that the likelihood of pregnancy was higher with an endometrial thickness ranging from 8 to 14mm compared to thicknesses under 8mm, a difference that was statistically significant\u003csup\u003e[24]\u003c/sup\u003e. Research conducted by Zhao et al. on 1933 patients undergoing IVF-ET identified an endometrial thickness threshold of 7mm, below which the probability of pregnancy significantly declined\u003csup\u003e[25]\u003c/sup\u003e. These findings underscore the importance of endometrial thickness as a determinant of the quality of endometrial receptivity, suggesting that receptivity is markedly enhanced at thicknesses of 8 to 14 mm and substantially diminished when thickness falls below 7 mm. In this study, the mean endometrial thickness in the focal AM group was not significantly different from that in the control group, whereas the mean thicknesses in the diffuse and mixed AM groups were notably lower than in the control group. Specifically, the average thickness in the diffuse AM group was less than 8mm, representing a statistically significant reduction compared to the control group. The mean thickness in the mixed AM group was 6.1mm, not only lower than that of the control group but also significantly reduced compared to the other two AM groups, indicating that different ultrasonic types of AM exert varying effects on endometrial thickness. Focal AM had minimal impact on thickness, while diffuse and mixed AM were associated with significant thinning of the endometrium, particularly pronounced in mixed AM. This variation may be attributed to the size and location of lesions: focal AM lesions are typically located in the outer myometrium and exert minimal influence on the endometrium, while diffuse or mixed AM lesions, being closer to the endometrium, potentially have a more significant impact. Moreover, mixed AM is often accompanied by substantial adenomyoma, leading to severe uterine deformation and pronounced endometrial thinning\u003csup\u003e[22]\u003c/sup\u003e. Both endometrial thickness and EV reflect the general dimensions of the uterine cavity, with endometrial thickness also indicative of EV to a degree. The patterns of EV variation and inter-group differences observed in this study paralleled those of endometrial thickness, suggesting that the impact of different ultrasonic types of AM on endometrial thickness is akin to their effect on EV. Furthermore, the study demonstrated a significant reduction in the proportion of type A endometrium and an increase in type C endometrium in the AM groups compared to the control group, with no significant differences in endometrial classification within the AM groups. Endometrial classification is reflective of the pre-implantation uterine environment, types B and C suggest a premature closure of the \u0026quot;embryo implantation window,\u0026quot; unfavorable for subsequent embryo implantation\u003csup\u003e[27]\u003c/sup\u003e. Therefore, we think that AM disrupts the synchrony between the endometrium and the embryo by affecting the \u0026quot;embryo implantation window\u0026quot;, thereby impacting endometrial receptivity. Additionally, some researchers propose that alterations in endometrial classification are closely linked to hormonal levels\u003csup\u003e[28]\u003c/sup\u003e, with disturbances in estrogen and progesterone levels among AM patients contributing to changes in endometrial classification.\u003c/p\u003e\n\u003cp\u003eEndometrial and myometrial blood flow are commonly employed ultrasound parameters for evaluating endometrial receptivity. The endometrial blood flow score facilitates a semi-quantitative assessment of endometrial perfusion. VI, FI, and VFI represent advanced observational metrics introduced with technological advancements in ultrasound, offering quantitative evaluation of endometrial perfusion with enhanced precision and significant clinical relevance. This study\u0026apos;s findings revealed that within the case group, the occurrence of diffuse and mixed AM with endometrial blood flow scores of 3 and 2 was markedly lower compared to the control group, while scores of 0 and 1 were significantly more frequent, and VI, FI, and VFI values were also considerably reduced in comparison with the control group. Conversely, focal AM exhibited no significant differences from the control group in both semi-quantitative and quantitative measures of endometrial blood flow. This indicates that diffuse and mixed AM significantly impair endometrial blood perfusion, corroborating the findings of Vlahos et al. \u003csup\u003e[29]\u003c/sup\u003e. Focal AM, however, exerts minimal impact on endometrial perfusion. Furthermore, no statistical significance was observed between diffuse and mixed AM in the aforementioned blood flow ultrasound evaluation metrics, suggesting that the effects of diffuse and mixed AM on endometrial perfusion are coincident. This similarity in impact could be attributed to the adenomyotic lesions within AM and the consequent compression of blood vessels, leading to diminished endometrial blood supply. In contrast, focal AM, due to its limited contact with the endometrium, has negligible influence on blood flow.\u003c/p\u003e\n\u003cp\u003eIn the evaluation of ultrasound indicators for the JZ and endometrial peristalsis, it was observed that the incidence of regular JZ appearances in the focal, diffuse, and mixed AM groups was significantly lower than in the control group, suggesting that AM contributes to the deterioration of JZ morphology in patients. Additionally, the study noted an elevated frequency of irregular and unclear JZ in the mixed and diffuse types compared with the focal type, while the occurrence of regular JZ in the mixed type was significantly diminished relative to both focal and diffuse types. This indicates a variability in the extent of JZ impairment across different ultrasonic classifications of AM, with a progressive increase in damage from focal to diffuse and mixed types. Rasmussen et al. have similarly highlighted that the JZ in AM patients is compromised\u003csup\u003e[30]\u003c/sup\u003e, aligning with the outcomes of this investigation, though their research did not differentiate between AM based on ultrasonic typology. The alteration in JZ is associated with the levels of ovarian hormones in patients, leading to the hypothesis that the varying degrees of JZ impairment in different ultrasonic types of AM may be linked to hormonal levels. This study also determined significant differences in endometrial motion between the diffuse and mixed AM groups compared to the control and focal AM groups, whereas endometrial peristalsis in focal AM was not significantly divergent from that in the control group.\u0026nbsp;The consensus among many researchers is that changes in endometrial peristalsis are attributable to abnormal JZ morphology\u003csup\u003e[31]\u003c/sup\u003e. In patients with AM, compromised JZ integrity results in altered endometrial peristalsis. Our findings suggest that focal AM-associated JZ morphology lesions do not markedly affect endometrial peristalsis, implying that alterations in JZ do not invariably lead to peristalsis abnormalities, potentially due to the extent of JZ damage. Recent studies indicate that AM may induce increased myometrial stiffness \u003csup\u003e[32]\u003c/sup\u003e, and abnormal myometrial stiffness could alter myometrial layer peristalsis, thereby influencing endometrial peristalsis. The specific impact of AM on endometrial peristalsis remains to be fully elucidated, necessitating further investigation.\u003c/p\u003e\n\u003cp\u003eNotably, this study found no significant differences in uterine artery PI values among the four groups, suggesting that AM might not affect uterine arterial blood flow in patients. Contrarily, some researches show that AM could elevate PI values by increasing uterine arterial blood flow\u003csup\u003e[33]\u003c/sup\u003e. Given reports of uterine artery blood flow parameters varying across menstrual cycles\u003csup\u003e[34]\u003c/sup\u003e, it is considered that these findings may relate to the timing of the study, warranting additional research for validation.\u003c/p\u003e\n\u003cp\u003eUltrasound serves not only as a prevalent diagnostic tool for AM but also as a means to assess endometrial receptivity. Currently, investigations into the endometrial receptivity of AM categorized by different ultrasonic types are limited. Earlier studies focusing on the ultrasound evaluation of endometrial receptivity often relied on a solitary indicator. Recent research findings suggest that the precision of using a single parameter to evaluate endometrial receptivity falls short compared to an association of multiple indicators, offering a more holistic assessment of the endometrial state and furnishing clinicians with more reliable diagnostic data\u003csup\u003e[35]\u003c/sup\u003e. The endometrial receptivity ultrasound scoring system facilitates the association of numerous indicators, quantifying subjective assessments to yield more objective and comprehensive outcomes, thereby establishing itself as a dependable evaluation technique. The scoring system employed in this investigation, refined from the Applebaum scoring method and integrated with findings from previous studies, aligns more closely with clinical practice and is logically sound. Utilizing an modified \u0026nbsp;endometrial receptivity ultrasound scoring system, this study assigned scores to patients with various ultrasonic types of AM. The outcomes indicated that the control group achieved the highest overall score, with the mixed AM group registering the lowest comprehensive score, followed by the diffuse and focal types, respectively, with each pairwise comparison reaching statistical significance. This underscores that AM impairs endometrial receptivity, with varying degrees of receptivity damage across different ultrasonic classifications of AM, and a progressive increase in damage severity from focal to diffuse and mixed AM. Scholars have previously noted that the endometrial receptivity in diffuse AM is inferior to that in focal AM\u003csup\u003e[36, 37]\u003c/sup\u003e, aligning with the findings of this study. However, given the categorization differences, prior research on AM\u0026apos;s impact on endometrial receptivity predominantly covered the focal and diffuse types, with no studies specifically addressing the ultrasound evaluation of endometrial receptivity in mixed AM. Mixed AM, embodying both focal and diffuse traits, typically manifests in advanced stages of the condition, which may elucidate the most pronounced impact on endometrial receptivity observed in mixed AM.\u003c/p\u003e\n\u003cp\u003eIn conclusion, adenomyosis compromises endometrial receptivity through alterations in endometrial morphology, thickness, classification, intimal blood flow index, JZ, endometrial peristalsis, among other factors. The indices of endometrial receptivity impairment and the extent of damage vary across different ultrasonic classifications of adenomyosis. The endometrial receptivity ultrasound scoring system addresses the limitations of relying on a single ultrasound parameter and presents an effective method for assessing endometrial receptivity. Analysis using the modified endometrial receptivity ultrasound scoring system for various ultrasonic types of adenomyosis revealed that the endometrial receptivity in cases of mixed adenomyosis was significantly inferior compared to the other two types, with the receptivity in diffuse adenomyosis being lower than in focal adenomyosis. Thus, it is advisable to perform comprehensive transvaginal ultrasound examinations and ultrasonic classifications for adenomyosis patients contemplating pregnancy. Should the ultrasound suggest mixed adenomyosis, clinicians are urged to undertake interventions to enhance the probability of successful pregnancy outcomes.\u003c/p\u003e"},{"header":"4. Conclusion","content":"\u003cp\u003eThe receptivity of the endometrium in patients with AM is diminished. The ultrasonic indices of endometrial receptivity impairment and the degree of damage vary among different ultrasonic types of AM, with mixed and diffuse AM showing particularly significant differences. Using the modified endometrial receptivity ultrasound scoring system to evaluate the endometrial receptivity of AM patients shows that the greatest reduction in endometrial receptivity is observed in patients with mixed AM, succeeded by those with diffuse AM, and least in those with focal AM.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthors\u0026apos; contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eKailing Tan：Conceptualization, Data curation, Writing\u0026ndash;original draft\u003c/p\u003e\n\u003cp\u003eYifang Ye：Formal analysis, Investigation, Writing\u0026nbsp;\u0026ndash;\u0026nbsp;original draft\u003c/p\u003e\n\u003cp\u003eJiemin Chen、Yaqian Zhang：Software, Resources, Writing\u0026nbsp;\u0026ndash;\u0026nbsp;review \u0026amp; editing\u003c/p\u003e\n\u003cp\u003eQiuyue Chen: Methodology, Project administration, Writing\u0026nbsp;\u0026ndash;\u0026nbsp;review \u0026amp; editing\u003c/p\u003e\n\u003cp\u003eGuorong Lyu: Supervision, Validation, Visualization, Writing\u0026nbsp;\u0026ndash;\u0026nbsp;review \u0026amp; editing\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding Statement:\u0026nbsp;\u003c/strong\u003eThis study was supported by the Fujian Provincial Department of Science and Technology (NO. 2019J01478).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData Availability\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe raw data supporting the conclusions of this article will be made available by the authors on request.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthics approval and consent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe study was approved by the Ethics Committee of the Second Affiliated Hospital of Fujian Medical University\u0026nbsp;(NO. 2023-272), All participants were informed about the study protocol and provided written informed consent to participate in the study. I confirm that all methods were performed in accordance with the relevant guidelines. All procedures were performed inaccordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent to Publish declaration\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003enot applicable\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare no competing interests.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eHarada T, Taniguchi F, Guo SW, Choi YM, Biberoglu KO, Tsai SS, et al. The Asian Society of Endometriosis and Adenomyosis guidelines for managing adenomyosis[J].\u003cem\u003e \u003c/em\u003eReprod Med Biol, 2023,22:e12535.\u003c/li\u003e\n\u003cli\u003eYang Naiping, Xu Hong, Gu Nihao. 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Ultrasound Elastography for the Diagnosis of Endometriosis and Adenomyosis: A Systematic Review with Meta-analysis[J].\u003cem\u003e \u003c/em\u003eUltrasound Med Biol, 2023,49:699-709.\u003c/li\u003e\n\u003cli\u003eJeng CJ, Ou KY, Long CY, Chuang L, Ker CR. 500 cases of high-intensity focused ultrasound (HIFU) ablated uterine fibroids and adenomyosis[J].\u003cem\u003e \u003c/em\u003eTaiwan J Obstet Gynecol, 2020,59:865-71.\u003c/li\u003e\n\u003cli\u003eDogan O, Yildiz A, Temizkan O, Pulatoglu C. Comparison of uterine, endometrial and ovarian blood flow by transvaginal color doppler ultrasound in ovulatory and anovulatory cycles[J].\u003cem\u003e \u003c/em\u003eGinekol Pol, 2016,87:581-4.\u003c/li\u003e\n\u003cli\u003eWang Xiaoxuan. Evaluation of endometrial receptivity in patients with freeze-thaw embryo transfer by ultrasonic multimodal scores [D]. Shandong University. 2023.\u003c/li\u003e\n\u003cli\u003eTamura H, Kishi H, Kitade M, Asai-Sato M, Tanaka A, Murakami T, et al. 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Clinical outcomes of infertility treatment for women with adenomyosis in Japan[J].\u003cem\u003e \u003c/em\u003eReprod Med Biol, 2017,16:276-82.\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003eTables 1 to 5 are available in the Supplementary Files section.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"adenomyosis, ultrasound, endometrial receptivity, score","lastPublishedDoi":"10.21203/rs.3.rs-8194490/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-8194490/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003ePurpose\u003c/h2\u003e\u003cp\u003eTo study the efficacy of multimodal ultrasonography in evaluating endometrial receptivity in patients presenting with various ultrasonic manifestations of adenomyosis (AM).\u003c/p\u003e\u003ch2\u003eMethods\u003c/h2\u003e\u003cp\u003eA total of 100 patients diagnosed with AM were categorised into three subgroups: 26 with focal AM, 40 with diffuse AM, 34 with mixed AM. A control group comprised 44 healthy females. All participants underwent transvaginal ultrasound between the 10th and 14th day of their normal menstrual cycle.Measurements included endometrial thickness, uterine artery pulsatility index (PI), endometrial classification, blood perfusion, intima-muscular junction zone (JZ), direction of endometrial peristalsis, endometrial volume (EV), vascular index (VI), flow index (FI), and vascular blood flow index (VFI). A modified endometrial receptivity ultrasound scoring system was devised, and differences in these ultrasound indices and comprehensive endometrial receptivity scores across the four groups were analysed.\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e\u003cp\u003eExcept for uterine artery PI, statistically significant differences were observed across the four groups in terms of intima thickness, EV, intima type, intima blood flow score, VI, FI, VFI, JZ, intima peristalsis, and comprehensive endometrial receptivity scores(all \u003cem\u003eP\u003c/em\u003e\u0026thinsp;\u0026le;\u0026thinsp;0.01). Comprehensive scores of endometrial receptivity were sequentially lower in the control group, focal AM group, diffuse AM group, mixed AM group, with each pairwise comparison being statistically significant (\u003cem\u003eP\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.05).\u003c/p\u003e\u003ch2\u003eConclusions\u003c/h2\u003e\u003cp\u003eEndometrial receptivity in patients with AM is compromised. The refined endometrial receptivity ultrasound scoring system offers a comprehensive assessment of endometrial receptivity in AM patients, the severity of endometrial receptivity impairment is most pronounced in patients with mixed AM, followed by diffuse AM, and least in focal AM.\u003c/p\u003e","manuscriptTitle":"Multimodal ultrasound in evaluation of the endometrial receptivity in patients with different ultrasonic classifications of AM","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-12-11 00:42:58","doi":"10.21203/rs.3.rs-8194490/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"92765ad7-edde-4306-9557-3d3d1f7ddf82","owner":[],"postedDate":"December 11th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2026-04-28T07:55:09+00:00","versionOfRecord":[],"versionCreatedAt":"2025-12-11 00:42:58","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-8194490","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-8194490","identity":"rs-8194490","version":["v1"]},"buildId":"B-jG_2CBjPDmsCi4Wdhf-","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}