A persistent diagnostic gap: awareness and workup of bleeding disorders in heavy menstrual bleeding among Dutch gynecologists and hematologists

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Luijten, S. Groenen, L. Nieuwenhuizen, M. Y. Bongers, J. C. Leemans, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-8310699/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 06 Apr, 2026 Read the published version in BMC Women's Health → Version 1 posted 15 You are reading this latest preprint version Abstract Background Heavy menstrual bleeding (HMB) is common in the general population, affecting at least one-quarter of women of reproductive age. A bleeding disorder has been reported as an underlying cause of HMB in 30% of hospital-seen cases suffering from HMB. Despite this, bleeding disorders appear to be substantially underdiagnosed in HMB. Our primary objective is to evaluate the awareness and diagnostic work up regarding bleeding disorders in patients with HMB among gynecologists and hematologists in the Netherlands. Methods An online questionnaire was conducted in 2023. The survey was distributed by email, with an anonymous link to 1508 gynecologists and 646 hematologists. Results Of the 2154 emails sent, 261 surveys were analyzed: 149 from gynecologists and 62 from hematologists representing a 10% response rate. Most gynecologists (89%) estimated the prevalence of bleeding disorders in HMB to be below 15%, with 40% under 5%. In comparison, the majority of hematologists (77%) placed their estimate between 5%-30%. Screening tools, including pre-visit questionnaires, anamnestic or laboratory evaluation, were not structurally used by gynecologists. Only 5% of gynecologists reported participating in multidisciplinary team meetings on bleeding disorders and HMB, compared to 34% of hematologists. Moreover, 94% of responding gynecologists reported seldom or never referring HMB patients to a hematologist. Conclusions This study highlights the underestimation of the prevalence of bleeding disorders among patients with HMB. Systematic screening for bleeding disorders in patients with HMB by gynecologists is largely lacking. These findings underscore the necessity of increasing awareness of bleeding disorders and to implement a structured diagnostic workup of HMB. women’s health heavy menstrual bleeding bleeding disorders awareness Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Background Heavy menstrual bleeding (HMB) is common in the general population and affects at least one-quarter of women in reproductive age (1). According to the Federation of Gynecology and Obstetrics (FIGO), HMB is characterised as menstrual blood loss that negatively affects a woman's physical, emotional, social, or material quality of life, and is linked to significant economic costs (2–4). HMB may result from various underlying pathologies. The PALM-COIEN classification system was developed to categorize the different underlying causes (5): Polyps, adenomyosis, leiomyoma, malignancy and hyperplasia represent structural causes and, coagulopathy, ovulatory dysfunction, endometrial, iatrogenic and unclassified representing entities that cannot be visibly defined by ultrasound or MRI. Systemic disorders of hemostasis are included under the heading of coagulopathy. HMB is a leading cause of gynecological consultations in both primary and secondary healthcare settings (6). A bleeding disorder is rarely considered in the differential diagnosis of HMB (7). However, a recent systematic review and meta-analysis demonstrates an overall prevalence of bleeding disorders of 30% in hospital-seen cases of adults presenting with HMB (8). In an adolescent HMB population, a prevalence of 19.4% for underlying bleeding disorders has been demonstrated (9). The most common bleeding disorder in HMB is von Willebrand’s disease, with a prevalence ranging from 5% to 24% (10). Platelet disorders, factor deficiencies, and hemophilia carriership are also associated with HMB. Recognising the presence and severity of bleeding disorders is a fundamental step in the management of HMB patients. An accurate diagnosis is essential to protect for potential bleeding risks in surgery or during delivery and to protect women for unnecessary HMB treatments like endometrial ablation or hysterectomy (11, 12). Moreover, diagnosis supports family awareness in hereditary cases and affirms patients’ experiences. Nevertheless, in European heamophilia treatment centers, alghorithms for managing HMB are lacking and there is a need for effective multidisciplinary management of HMB (13). Diagnosing a bleeding disorder can be complicated and needs specific expertise. The Dutch Society of Obstetrics and Gynecology (NVOG) recommends to not routinely screen for von Willebrand disease in cases of HMB, and does not provide guidance on how to screen for bleeding disorders (14). We set up this study to gain insight into the awareness and diagnostic work of underlying bleeding disorders in HMB. The primary objective of this study is to evaluate the awareness and diagnostic work up regarding underlying bleeding disorders in patients with HMB among gynecologists and hematologists in the Netherlands. We aimed to establish whether gynecologists and hematologists are aware of the prevalence of underlying bleeding disorders in patients suffering from HMB, whether gynecologists utilize screening tools to identify women suspected of having a bleeding disorder, whether laboratory testing in this context is performed by gynecologists and whether HMB patients are referred to hematologists for further evaluation of potential underlying bleeding disorders. Methods An online questionnaire was developed using web-based platform Qualtrics XM. The Medical Ethics Committee of Máxima Medical Centre (MMC) reviewed the study and confirmed that the Medical Research Involving Human Subjects Act (WMO) does not apply to this study. The Local Feasibility Research Committee at MMC granted feasibility approval (2023-MMC-056). The questionnaire was developed based on the expertise of a working group consisting of fifteen expert researchers and gynecologists specialized in benign gynecology or hematology, as well as three hematologists. A draft version of the questionnaire was presented to the working group, and subsequently revised based on their recommendations. Two distinct versions of the questionnaire were developed and distributed; one tailored for gynecologists and one for hematologists. The questionnaire was distributed to all gynecologists, hematologists and residents registered with either NVOG (n = 1508) or the Dutch Association for Hematologists (NVVH) (n = 646). This email invitation included a cover letter explaining the study and a link to the survey. To broaden our reach, a QR code linking to the survey was also distributed at relevant work groups. Respondents were included between June and October 2023. Due to the anonymity of participation, it was not possible to determine the respondents’ affiliated centers. Multiple respondents from the same centre could participate. The questionnaire for gynecologists consisted of 22 questions, while the questionnaire for hematologists consisted of 19 questions. It consisted primarily of multiple-choice questions with some including an “Other, please specify” option for free-text responses, and concluded with an open-ended question inviting additional comments or suggestions. The open-ended responses were reviewed but did not yield relevant insights: therefore no formal quantitative analysis was performed. The survey was divided in three sections: general information (1), organization of care (2) and analysis and diagnostics in HMB with a specific focus on underlying bleeding disorders (3 ) (see Supplementary data for complete questionnaires ). We analyzed respondents who confirmed to be a gynecologist, hematologist or resident in one of these working fields and who completed at least 90% of the questions. Questionnaires were considered invalid if the questionnaire was left blank, or if the respondent was working in another specialty. Questionnaires were considered incomplete and excluded from analysis if > 10% of the close-ended questions were left unanswered. An HMB clinic was defined as a department where patients with HMB can typically undergo a see-and-treat process. A screening tool was defined as the use of a bleeding history, a family history with attention for bleeding disorders or the application of the International Society on Thrombosis and Hemostasis Bleeding Assessment Tool (ISTH BAT). Gynecologists were asked about the laboratory tests they request using the question: ‘Do you use laboratory tests in the context of bleeding disorders in cases of heavy menstrual bleeding?’, with the following possible answers: never, seldom, regularly, often or always. This was followed by the question: ‘Do you use a fixed set of laboratory tests for analysis?’ Followed by: ‘Which laboratory tests do you use in the first step?’ (multiple answers allowed). Statistical analysis Data was extracted from Qualtrics and imported into Statistical Packages for Social Sciences (SPSS). The statistical analyses were performed with International Business Machines Corporation (IBM) SPSS statistics version 29. Descriptive statistics were employed on all variables. Results A total of 261 (12,1%) surveys were returned. 181 (69,3%) respondents were working in the field of gynecology and 80 (30,7%) respondents were working in the field of hematology. The analyses were limited to 211 surveys, as 19 surveys were stated invalid: 18 surveys were not filled in, one survey was filled in by a respondent working in another specialism. Moreover, 31 surveys were incomplete and excluded (Fig. 1 ). Of the 211 included questionnaires, 149 surveys were completed by gynecologists (71%) and 62 by hematologists (29%). The characteristics of the respondents are shown in Table 1 . Gynecologists were involved in the following sub-specialties (multiple options per respondent possible); 117 benign gynecology (79%), 66 obstetrics (44%), 41 fertility (28%), 48 uro-gynecology (32%) and 40 oncologic gynecology (27%). Of all participating hematologists, 20 (32%) were employed at a hemophilia treatment center. 97% of gynecologists reported to manage HMB on a regular basis, compared to 60% of hematologists. In total 13% of respondents (28/211) participated in a multidisciplinary team discussion about bleeding disorders wherein HMB patients are discussed. This was more common among hematologists (34%) than gynecologists (5%). Table 1 Characteristics of respondents Characteristics Gynecologists n = 149 Hematologists n = 62 Gynecologist 117 (78.5%) Resident gynecology 32 (21.5%) General internal medicine specialist 3 (4.8%) Internist-hematologist 52 (83.9%) Internist vascular medicine 2 (3.2%) Resident internal medicine 5 (8.1%) Hospital type University hospital 19 (12.8%) 18 (29.0%) General teaching hospital 88 (59.0%) 36 (58.1%) General non-teaching hospital 35 (23.5%) 8 (12.9%) Independent treatment centre 7 (4.7%) 0 (0%) Focussed HMB clinic present Yes 30 (20.1%) 9 (14.5%) No 119 (79.9%) 53 (85.5%) Structured multidisciplinary team discussion regarding bleeding disorders and HMB Yes 7 (4.7%) 21 (33.9%) No 142 (95.3%) 41 (66.1%) Values are n (%) Estimated prevalence of underlying bleeding disorders in HMB The estimates of the prevalence of bleeding disorders as the cause of HMB varied among respondents (Fig. 2 ). Most respondents selected categories below the literature-based prevalence of 30% (8). The majority of gynecologists (89%) estimated a prevalence below 15%, with 40% placing it under 5%. In comparison, 63% of hematologists estimated the percentage to below 15%, and the majority of hematologists (77%) estimated it to be between 5–30%. In respondents who have a focussed HMB clinic present (n = 39), no difference was seen in the estimated prevalence of underlying bleeding disorders in HMB compared to those without such a clinic. * Reported prevalence of underlying bleeding disorders in HMB according to the literature is 30% (8) Definition HMB by hematologists In order to assess which characteristics hematologists consider associated with HMB, and to explore the potential for alignment with gynecologists’ definitions, hematologists were asked to select all relevant characteristics. Almost all symptoms were chosen in over 60% of the cases except for “losing clots” and “PBAC score > 100” (Table 2 ). Table 2 Characteristics associated with HMB by hematologists HMB symptom N = 61 Menstruation during > 7 days 43 (71%) Changing pads more often than every two hours 54 (89%) Losing clots 26 (43%) PBAC score > 100 24 (39%) Work/school omission 46 (75%) Hormonal therapy related to HMB 39 (64%) Iron deficiency anemia 39 (64%) Need for iron supplementation 45 (72%) Need for blood transfusion 57 (93%) Values are n (%), characteristics were based on HMB ACOG and NICE guidelines, as well as the ISTH-BAT questionnaire(15, 16) Screening tool: pre-visit questionnaire Table 3 provides an overview of the pre-visit questionnaires used by gynecologist and hematologists (multiple options possible). The majority of respondents indicated that no questionnaires were send to patients prior to the consultation. Among gynecologists and hematologists, respectively 20% and 9% reported using any form of questionnaire. The ‘PBAC/menstruation calendar” and a ‘self-developed questionnaire’ were most commonly used by gynecolgists. A ‘self-developed questionnaire’ was not further defined. Table 3 Questionnaires before visit, multiple options possible Questionnaire Responding gynecologists n = 149 Responding hematologists n = 58 No questionnaire 120 (80%) 53 (91%) Questionnaire 29 (20%) 5 (9%) PBAC/menstruation calendar # 17 (11%) 2 (3%) ISTH-BAT # 0 (0%) 4 (7%) Self-BAT # 0 (0%) 0 Self-developed questionnaire # 15 (10%) 0 Different questionnaire* # 6 (4%) 2 (3%) Values are n (%) PBAC = Pictorial Blood Loss Assessment Chart, ISTH-BAT = International Society on Thrombosis and Hemostasis Bleeding Assessment Tool, Self-BAT = self Bleeding Assessment Tool *intake questionnaire, decision aid, uterine fibroid symptom and quality of life questionnaire or general hospital questionnaire. # Respondents could give multiple answers Screening tool: anamnestic and laboratory evaluation While respondents working as gynecologists (n = 149) did not routinely inquire about bleeding history or a family history of bleeding disorders, more than 80% (52/62 and 49/62) of hematologist respondents reported that they consistently ask about these aspects (Fig. 3). A bleeding score (ISTH BAT) is never used by 75% (112/149) of gynecologist respondents. Only 6% of gynecologists reported frequently using laboratory tests to detect bleeding disorders. Figure 3. Anamnestic and laboratory evaluation practices among gynecologists and hematologists *responding gynecologists n = 149 for bleeding history, family history in the context of bleeding disorders, and bleeding score (ISTH BAT, n = 145 for laboratory evaluation in the context of bleeding disorders. Responding hematologists n = 62. Laboratory testing in the context of bleeding disorders A total of 145 gynecologists responded to the question ‘which laboratory tests do you use in the first step? (multiple options possible)’. When performing laboratory testing, most gynecologists initially requested hemoglobin/hematocrit (132/145), ferritin (78/145) and von Willebrand activity (75/145). Common laboratory tests requested by hematologists are platelet count (62/62), hemoglobin/hematocrit (61/62), prothrombin time, activated partial thromboplastin time (60/62) and von Willebrand activity (51/62). Figure 4 shows an overview of the laboratory tests performed. Hb/Ht = Hemoglobin(Hb)/Hematocrit, PT = Prothrombin time, APTT = Activated partial thromoplastin time, PFA = Platelet function assay Referral to a hematologist Of 149 respondents who work as a gynecologist, 26 reported that they ‘never’ refer patients with HMB to a hematologist, 114 gynecologists refer ‘seldom’, 7 refer ‘regularly’ and 2 refer ‘often’. None of the responders reported to ‘always’ refers patients. Figure 5 provides an overview of all referral rates. Guideline HMB We finally analyzed whether gynecologists believe that the Dutch guideline for HMB (NVOG), gynecologists provide sufficient information on background and diagnostics of bleeding disorders as this may influence awareness and clinical practice. Of the respondents, 49% reported the information as insufficient. Discussion Main findings Our study evaluated the awareness and diagnostic work up regarding underlying bleeding disorders in patients with HMB among gynecologists and hematologists in the Netherlands. Both groups substantially underestimated the evidence-based prevalence of 30% (8), although hematologists provided estimates closer to the reported prevalence. Pre-visit questionnaires were rarely used, and gynecologists did not apply screening tools to identify an increased risk of an underlying bleeding disorder in HMB (i.e. BAT questionnaires) prior to consultation. During or after consultation, gynecologists scarcely applied anamnestic (e.g. the ISTH BAT) and laboratory evaluation aimed at identifying bleeding disorders. Moreover, 94% of responding gynecologists seldom or never refer HMB patients to a hematologist for further analysis, which aligns with their perception of low prevalence. Interpretation The underestimation of the prevalence, low referral rate, and infrequent use of anamnestic and diagnostic evaluation among gynecologists demonstrates limited awareness or prioritization of bleeding disorders in the evaluation of HMB. Similarly, hematologists tend to underestimate the prevalence of bleeding disorders in HMB. Despite the need for effective multidisciplinary management of HMB (13, 17), only 13% of respondents participate in a multidisciplinary team discussion about bleeding disorders and HMB. Together this may lead to missed opportunities for timely diagnosis and treatment. Moreover, undiagnosed bleeding disorders can lead to inappropriate treatment, unnecessary procedures (endometrial ablation, hysterectomy), and preventable complications in trauma, surgery or childbirth (11, 12). The limited awareness may be partly attributable to the current Dutch HMB guideline, which according to 49% of responding gynecologists, provides limited guidance on how to screen for bleeding disorders. Its main focus is to screen for anatomical/structural disorders as a cause of HMB (14). The lack of clear guidelines may stem from the limited high-quality evidence on effective screening strategies available to gynecologists. We moreover found that multidisciplinary team meetings on bleeding disorders and HMB are uncommon in the Netherlands, which may further contribute to low awareness, and limited referrals and diagnostic evaluation. This warrants attention as Curry et al. demonstrated that 90% of women with inherited bleeding disorders consider a multidisciplinary model as beneficial (17). Similarly, van Galen et al. conclude the need for effective multidisciplinary management of HMB in bleeding disorders (13). Hematologists also underestimate the prevalence of bleeding disorders in women with HMB, and show gaps in recognizing symptoms that indicate HMB. This may partly explain previous findings that HMB is underestimated in hemophilia treatment centers (13). Aligning definitions between hematologists and gynecologists may support more consistent interpretation and communication in multidisciplinary settings, even though we found that multidisciplinary discussions on HMB and bleeding disorders are not routinely implemented. Pre-visit questionnaires are scarcely used by hematologists and the self-BAT is never applied despite validation studies (18). Hematologists however, frequently use the ISTH-BAT during consultations. Notably, 7% of hematologist respondents send this questionnaire to their patients prior to consultation despite it is designed as a physician-administered questionnaire. Our study demonstrates that awareness has remained largely unchanged over the past two decades. Surveys among gynecologists in the US (2002) and UK (2006) revealed that bleeding disorders were considered rare causes of HMB, with only 4% of US respondents considering von Willebrand disease (7) and most UK respondents estimating its prevalence at < 1% (19). Indeed, women with bleeding disorders remain underrecognized and underdiagnosed worldwide, reflecting longstanding gender bias in care (20). This underdiagnosis may be partly due to a lack of consensus who to screen for bleeding disorders in HMB. Our findings indicate that screening tools to identify HMB patients suspected of having a bleeding disorder are hardly used. Even when a gynecological cause for HMB is identified, clinicians should consider the possibility of a coexisting bleeding disorder, as these conditions are not mutually exclusive (21). Several international guidelines recommend screening individuals presenting with HMB for a potential bleeding disorder. However, these guidelines lack consistency in their recommendations. The American College of Obstetricians and Gynecologists (ACOG) offers a committee opinion (2019) on screening HMB adolescents (15). They recommend to identify risk factors for bleeding disorders when obtaining a medical history, and suggest using the adapted Philipp screening tool (2011) (22). The National Institute for Health and Care Excellence (NICE) recommends to consider testing for bleeding disorders in women who present with HMB since menarche, and having a personal or family history suggesting a bleeding disorder (6). In our study, 30% of responding gynecologists reported routinely assessing a personal bleeding history, whereas 40% indicated that they rarely inquire about a family history suggestive for a bleeding disorder. The NVOG currently advises against routine screening for von Willebrand disease in cases of HMB, and provides no further guidance on how to screen for bleeding disorders in this context (14). Consequently, it is not surprising that laboratory testing to detect bleeding disorders is rarely used by gynecologists in HMB patients. In our survey, only 6% of gynecologist respondents indicated that they often use laboratory testing for bleeding disorders. Comprehensive coagulation tests are moreover not routinely available in general hospitals in the Netherlands. Combined with limited awareness and weak collaboration with hematology department, this likely explains the limited laboratory evaluation observed. Previous studies confirm limited laboratory testing. An Australian retrospective audit showed that 40–54% of women with HMB who attended a tertiary women’s hospital and were at risk of having a mild bleeding disorder were not tested for (23). In post-pubertal girls and adolescents with HMB, von Willebrand disease screening occurred in only 8% of cases and 16% of severe (24). Similarly, a UK survey reported that just 12% of gynecologists would arrange testing an 18-year-old with HMB for von Willebrand disease, and only 2% would test a 35-year-old [16]. In our study, 94% of responding gynecologists rarely or never referred to a hematologist for further evaluation of the coagulation system. This is in line with the study of Dilley et al. in 2002 who demonstrated that only 3% of surveyed American gynecologists refer HMB patients to other specialists (7). The persistence of such low referral rates over decades suggests systemic gaps in interdisciplinary collaboration. Strengths & limitations A major strength of this study is the nationwide scope, including both gynecologists and hematologists, providing complementary perspectives on the diagnostic approach to bleeding disorders in HMB patients. Moreover, the survey addressed not only perceived prevalence but also evaluation and referral practices, highlighting awareness and practice gaps as key targets for improving care pathways. Additionally, the survey is developed and refined in collaboration with an expert group, which ensured that the questions were clearly formulated and that the response options closely reflected daily practice. Several limitations should be acknowledged. First, due to anonymity, center-level comparisons could not be made, and findings are based on self-reported practices rather than observed behavior. Second, volunteer bias may have influenced the results. Physicians with a particular interest or involvement in this subject are likely overrepresented in the sample, which may limit the representativeness of Dutch gynecologists and hematologists managing HMB. These respondents may have been more knowledgeable or attentive in completing the questionnaire, potentially leading to an overestimation of best practices. Finally, of all notified practitioners, only 9.8% of gynecologists and 9.5% of hematologists in the Netherlands were included. Future studies Future studies should focus on strategies to increase awareness of bleeding disorders as an underlying cause of HMB, as this is essential for appropriate referral and a timely diagnosis. In addition, research is essential to develop and validate efficient, practical screening tools that can be implemented in gynecology practice. These tools should aim to identify women with HMB at risk for bleeding disorders early in the diagnostic process. Finally, the development of a uniform international guideline for the assessment of bleeding disorders in HMB is warranted to reduce diagnostic delays, and improve diagnostic work-up and appropriate patient care. Conclusion Our study demonstrates that awareness of underlying bleeding disorders in women with HMB has remained largely unchanged over the past two decades. The prevalence is underestimated, particularly by gynecologists but also by hematologists, and referral rates remain low. Diagnostic work-up, including screening tools and laboratory testing is not routinely used by gynecologists, and structured multidisciplinary discussions are lacking in both specialities. These findings highlights the need for clearer guidelines, targeted education, practical screening tools, and stronger collaboration between gynecology and hematology. Abbreviations HMB heavy menstrual bleeding FIGO Federation of Gynecology and Obstetrics NVOG Dutch Society of Obstetrics and Gynecology MMC Máxima Medical Center WMO Medical Research Involving Human Subjects Act NVVH Dutch Association for Hematologists ISTH BAT International Society on Thrombosis and Hemostasis Bleeding Assessment Tool SPSS Statistical Packages for Social Sciences IBM International Business Machines Corporation ACOG American College of Obstetricians and Gynecologists NICE National Institute for Health and Care Excellence Declarations Ethics approval and consent to participate The Local Feasibility Research Committee at MMC granted feasibility approval (2023-MMC-056). This study involved an anonymous, voluntary online survey distributed to all gynecologists and hematologists in the Netherlands. Participation required respondents to actively open the survey link and complete the questionnaire. According to our Medical Ethics Committee (Máxima Medical Centre), the study did not fall under the Medical Research Involving Human Subjects Act (WMO), and written informed consent was therefore not required. Completion and submission of the anonymous questionnaire were considered to imply informed consent. Respondents were informed in the invitation email and at the start of the survey about the study purpose, voluntary participation, anonymity, and data handling. No identifiable personal data were collected. Consent for publication Not applicable. Availability of data and materials The datasets used and analyzed during the current study available from the corresponding author on reasonable request. Competing interests The authors declare that they have no financial interests or personal relationships that could have appeared to influence the work of this paper. Funding Not applicable. Author’s contributions S.L., L.N., M.Y.B., J.C.L. and P.M.A.J.G., conceptualized the study; S.L. was responsible for date collection; S.L. drafted the manuscript; S.G., L.N., M.Y.B., J.C.L., P.M.A.J.G. revised it critically for important intellectual content. All authors read and approved the final manuscript. References Fraser IS, Mansour D, Breymann C, et al. Prevalence of heavy menstrual bleeding and experiences of affected women in a European patient survey. International Journal of Gynaecology and Obstetrics: The Official Organ of the International Federation of Gynaecology and Obstetrics. 2015;128(3):196-200. Akiyama S, Tanaka E, Cristeau O, et al. Treatment patterns and healthcare resource utilization and costs in heavy menstrual bleeding: a Japanese claims database analysis. J Med Econ. 2018;21(9):853-860. Schoep ME, Adang EMM, Maas JWM, et al. Productivity loss due to menstruation-related symptoms: a nationwide cross-sectional survey among 32 748 women. 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J Womens Health Gend Based Med. 2002;11(1):39-44. Comishen KJ, Bhatt M, Yeung K, et al. Etiology and diagnosis of heavy menstrual bleeding among adolescent and adult patients: a systematic review and meta-analysis of the literature. J Thromb Haemost. 2025;23(3):863-876. Hall EM, Ravelo AE, Aronoff SC, Del Vecchio MT. Systematic review and meta-analysis of the etiology of heavy menstrual bleeding in 2,770 adolescent females. BMC Womens Health. 2024;24(1):136. Shankar M, Lee CA, Sabin CA, et al. von Willebrand disease in women with menorrhagia: a systematic review. BJOG. 2004;111(7):734-740. Kulkarni R. Improving care and treatment options for women and girls with bleeding disorders. Eur J Haematol. 2015;Dec:95 Suppl 81:2-10(1600-0609 (Electronic)). Sanigorska AA-O, Chaplin SA-O, Holland MA-O, et al. The lived experience of women with a bleeding disorder: A systematic review. Research and practice in thrombosis and haemostasis. 2022(2475-0379 (Electronic)). 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Haemophilia: The Official Journal of the World Federation of Hemophilia. 2021;27(4):e534-e536. Jacobson AE, Vesely SK, Koch T, et al. Patterns of von Willebrand Disease Screening in Girls and Adolescents With Heavy Menstrual Bleeding. Obstet Gynecol. 2018;131(6):1121-1129. Additional Declarations No competing interests reported. Supplementary Files Supplementaldataquestionnaires.docx Cite Share Download PDF Status: Published Journal Publication published 06 Apr, 2026 Read the published version in BMC Women's Health → Version 1 posted Editorial decision: Revision requested 27 Jan, 2026 Reviews received at journal 23 Jan, 2026 Reviewers agreed at journal 21 Jan, 2026 Reviews received at journal 18 Jan, 2026 Reviewers agreed at journal 18 Jan, 2026 Reviews received at journal 17 Jan, 2026 Reviewers agreed at journal 14 Jan, 2026 Reviews received at journal 14 Jan, 2026 Reviewers agreed at journal 14 Jan, 2026 Reviewers agreed at journal 09 Jan, 2026 Reviewers invited by journal 07 Jan, 2026 Editor invited by journal 15 Dec, 2025 Editor assigned by journal 11 Dec, 2025 Submission checks completed at journal 11 Dec, 2025 First submitted to journal 08 Dec, 2025 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Luijten","email":"data:image/png;base64,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","orcid":"","institution":"Máxima Medical Centre","correspondingAuthor":true,"prefix":"","firstName":"S.","middleName":"","lastName":"Luijten","suffix":""},{"id":571051496,"identity":"756b8aa2-b0f4-4ead-ab6d-e9300c3aa767","order_by":1,"name":"S. Groenen","email":"","orcid":"","institution":"Máxima Medical Centre","correspondingAuthor":false,"prefix":"","firstName":"S.","middleName":"","lastName":"Groenen","suffix":""},{"id":571051499,"identity":"674d872c-fea3-4eca-a05c-b385945962b2","order_by":2,"name":"L. Nieuwenhuizen","email":"","orcid":"","institution":"Máxima Medical Centre","correspondingAuthor":false,"prefix":"","firstName":"L.","middleName":"","lastName":"Nieuwenhuizen","suffix":""},{"id":571051501,"identity":"b3354540-175a-43a3-a4cd-703885bef636","order_by":3,"name":"M. Y. Bongers","email":"","orcid":"","institution":"Maastricht University","correspondingAuthor":false,"prefix":"","firstName":"M.","middleName":"Y.","lastName":"Bongers","suffix":""},{"id":571051504,"identity":"9be467c7-0079-4f5b-91e9-b4ea54b60d3f","order_by":4,"name":"J. C. 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06:10:35","extension":"html","order_by":11,"title":"","display":"","copyAsset":false,"role":"acdc-reference","size":73030,"visible":true,"origin":"","legend":"","description":"","filename":"earlyproof.html","url":"https://assets-eu.researchsquare.com/files/rs-8310699/v1/46d8775ddcff77442c0f0b92.html"},{"id":100011551,"identity":"65eb1346-fff5-4d79-bf6b-42c08f12d94b","added_by":"auto","created_at":"2026-01-12 06:10:39","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":72868,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eStudy flowchart\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-8310699/v1/50eaac735fc0b392719bebab.jpg"},{"id":100011531,"identity":"0e99ff26-d97e-4399-9645-25d687de800e","added_by":"auto","created_at":"2026-01-12 06:10:34","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":57800,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eEstimated prevalence of underlying bleeding disorders in women suffering HMB\u003c/strong\u003e \u003cstrong\u003ereported by gynecologists and hematologists\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cem\u003e* Reported prevalence of underlying bleeding disorders in HMB according to the literature is 30% (8)\u003c/em\u003e\u003c/p\u003e","description":"","filename":"2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-8310699/v1/e0fb7df98c21d72ca6e2651c.jpg"},{"id":100011519,"identity":"0e0c85b6-e0de-4b78-a39e-9b1cf35bc986","added_by":"auto","created_at":"2026-01-12 06:10:31","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":118408,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eAnamnestic and laboratory evaluation practices among gynecologists and hematologists\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cem\u003e*responding gynecologists n=149 for bleeding history, family history in the context of bleeding disorders, and bleeding score (ISTH BAT, n=145 for laboratory evaluation in the context of bleeding disorders. Responding hematologists n=62.\u003c/em\u003e\u003c/p\u003e","description":"","filename":"3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-8310699/v1/82017de8b38cd8f25a349452.jpg"},{"id":100011523,"identity":"deb78574-44c4-4eb3-99f5-7f6e8133ee47","added_by":"auto","created_at":"2026-01-12 06:10:31","extension":"jpg","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":100727,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eInitial laboratory testing by gynecologists (n=145) and hematologists (n=62)\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eHb/Ht = Hemoglobin(Hb)/Hematocrit, PT = Prothrombin time, APTT = Activated partial thromoplastin time, PFA = Platelet function assay\u003c/em\u003e\u003c/p\u003e","description":"","filename":"4.jpg","url":"https://assets-eu.researchsquare.com/files/rs-8310699/v1/815d97d8507ce56786c11673.jpg"},{"id":100011526,"identity":"2fed8719-ff7d-46da-965a-f0cb1e90864d","added_by":"auto","created_at":"2026-01-12 06:10:34","extension":"jpg","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":50454,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eReferral rate from gynecologist to hematologist of patients with HMB\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"5.jpg","url":"https://assets-eu.researchsquare.com/files/rs-8310699/v1/8ccbbfb313fb7d3f0e733652.jpg"},{"id":106810891,"identity":"bad60582-1a7a-4bf8-a81e-2a36d6bdc966","added_by":"auto","created_at":"2026-04-13 16:17:15","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1347397,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-8310699/v1/4bd219df-52e2-496c-bcf2-6f799c5b38ef.pdf"},{"id":100011540,"identity":"de359b8e-e8e4-4334-a780-3d84c0f9aadb","added_by":"auto","created_at":"2026-01-12 06:10:37","extension":"docx","order_by":0,"title":"","display":"","copyAsset":false,"role":"supplement","size":24127,"visible":true,"origin":"","legend":"","description":"","filename":"Supplementaldataquestionnaires.docx","url":"https://assets-eu.researchsquare.com/files/rs-8310699/v1/0bc8d76a406f646f0dca6f83.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"A persistent diagnostic gap: awareness and workup of bleeding disorders in heavy menstrual bleeding among Dutch gynecologists and hematologists","fulltext":[{"header":"Background","content":"\u003cp\u003eHeavy menstrual bleeding (HMB) is common in the general population and affects at least one-quarter of women in reproductive age (1). According to the Federation of Gynecology and Obstetrics (FIGO), HMB is characterised as menstrual blood loss that negatively affects a woman's physical, emotional, social, or material quality of life, and is linked to significant economic costs (2\u0026ndash;4). HMB may result from various underlying pathologies. The PALM-COIEN classification system was developed to categorize the different underlying causes (5): Polyps, adenomyosis, leiomyoma, malignancy and hyperplasia represent structural causes and, coagulopathy, ovulatory dysfunction, endometrial, iatrogenic and unclassified representing entities that cannot be visibly defined by ultrasound or MRI. Systemic disorders of hemostasis are included under the heading of coagulopathy. HMB is a leading cause of gynecological consultations in both primary and secondary healthcare settings (6). A bleeding disorder is rarely considered in the differential diagnosis of HMB (7). However, a recent systematic review and meta-analysis demonstrates an overall prevalence of bleeding disorders of 30% in hospital-seen cases of adults presenting with HMB (8). In an adolescent HMB population, a prevalence of 19.4% for underlying bleeding disorders has been demonstrated (9). The most common bleeding disorder in HMB is von Willebrand\u0026rsquo;s disease, with a prevalence ranging from 5% to 24% (10). Platelet disorders, factor deficiencies, and hemophilia carriership are also associated with HMB. Recognising the presence and severity of bleeding disorders is a fundamental step in the management of HMB patients. An accurate diagnosis is essential to protect for potential bleeding risks in surgery or during delivery and to protect women for unnecessary HMB treatments like endometrial ablation or hysterectomy (11, 12). Moreover, diagnosis supports family awareness in hereditary cases and affirms patients\u0026rsquo; experiences. Nevertheless, in European heamophilia treatment centers, alghorithms for managing HMB are lacking and there is a need for effective multidisciplinary management of HMB (13). Diagnosing a bleeding disorder can be complicated and needs specific expertise. The Dutch Society of Obstetrics and Gynecology (NVOG) recommends to not routinely screen for von Willebrand disease in cases of HMB, and does not provide guidance on how to screen for bleeding disorders (14). We set up this study to gain insight into the awareness and diagnostic work of underlying bleeding disorders in HMB. The primary objective of this study is to evaluate the awareness and diagnostic work up regarding underlying bleeding disorders in patients with HMB among gynecologists and hematologists in the Netherlands. We aimed to establish whether gynecologists and hematologists are aware of the prevalence of underlying bleeding disorders in patients suffering from HMB, whether gynecologists utilize screening tools to identify women suspected of having a bleeding disorder, whether laboratory testing in this context is performed by gynecologists and whether HMB patients are referred to hematologists for further evaluation of potential underlying bleeding disorders.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003eAn online questionnaire was developed using web-based platform Qualtrics XM. The Medical Ethics Committee of M\u0026aacute;xima Medical Centre (MMC) reviewed the study and confirmed that the Medical Research Involving Human Subjects Act (WMO) does not apply to this study. The Local Feasibility Research Committee at MMC granted feasibility approval (2023-MMC-056). The questionnaire was developed based on the expertise of a working group consisting of fifteen expert researchers and gynecologists specialized in benign gynecology or hematology, as well as three hematologists. A draft version of the questionnaire was presented to the working group, and subsequently revised based on their recommendations. Two distinct versions of the questionnaire were developed and distributed; one tailored for gynecologists and one for hematologists. The questionnaire was distributed to all gynecologists, hematologists and residents registered with either NVOG (n\u0026thinsp;=\u0026thinsp;1508) or the Dutch Association for Hematologists (NVVH) (n\u0026thinsp;=\u0026thinsp;646). This email invitation included a cover letter explaining the study and a link to the survey. To broaden our reach, a QR code linking to the survey was also distributed at relevant work groups. Respondents were included between June and October 2023. Due to the anonymity of participation, it was not possible to determine the respondents\u0026rsquo; affiliated centers. Multiple respondents from the same centre could participate. The questionnaire for gynecologists consisted of 22 questions, while the questionnaire for hematologists consisted of 19 questions. It consisted primarily of multiple-choice questions with some including an \u0026ldquo;Other, please specify\u0026rdquo; option for free-text responses, and concluded with an open-ended question inviting additional comments or suggestions. The open-ended responses were reviewed but did not yield relevant insights: therefore no formal quantitative analysis was performed. The survey was divided in three sections: general information (1), organization of care (2) and analysis and diagnostics in HMB with a specific focus on underlying bleeding disorders (3\u003cem\u003e)\u003c/em\u003e (see Supplementary data for complete questionnaires\u003cem\u003e).\u003c/em\u003e We analyzed respondents who confirmed to be a gynecologist, hematologist or resident in one of these working fields and who completed at least 90% of the questions. Questionnaires were considered invalid if the questionnaire was left blank, or if the respondent was working in another specialty. Questionnaires were considered incomplete and excluded from analysis if\u0026thinsp;\u0026gt;\u0026thinsp;10% of the close-ended questions were left unanswered. An HMB clinic was defined as a department where patients with HMB can typically undergo a see-and-treat process. A screening tool was defined as the use of a bleeding history, a family history with attention for bleeding disorders or the application of the International Society on Thrombosis and Hemostasis Bleeding Assessment Tool (ISTH BAT). Gynecologists were asked about the laboratory tests they request using the question: \u0026lsquo;Do you use laboratory tests in the context of bleeding disorders in cases of heavy menstrual bleeding?\u0026rsquo;, with the following possible answers: never, seldom, regularly, often or always. This was followed by the question: \u0026lsquo;Do you use a fixed set of laboratory tests for analysis?\u0026rsquo; Followed by: \u0026lsquo;Which laboratory tests do you use in the first step?\u0026rsquo; (multiple answers allowed).\u003c/p\u003e \u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analysis\u003c/h2\u003e \u003cp\u003eData was extracted from Qualtrics and imported into Statistical Packages for Social Sciences (SPSS). The statistical analyses were performed with International Business Machines Corporation (IBM) SPSS statistics version 29. Descriptive statistics were employed on all variables.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cp\u003eA total of 261 (12,1%) surveys were returned. 181 (69,3%) respondents were working in the field of gynecology and 80 (30,7%) respondents were working in the field of hematology. The analyses were limited to 211 surveys, as 19 surveys were stated invalid: 18 surveys were not filled in, one survey was filled in by a respondent working in another specialism. Moreover, 31 surveys were incomplete and excluded (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eOf the 211 included questionnaires, 149 surveys were completed by gynecologists (71%) and 62 by hematologists (29%). The characteristics of the respondents are shown in Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e. Gynecologists were involved in the following sub-specialties (multiple options per respondent possible); 117 benign gynecology (79%), 66 obstetrics (44%), 41 fertility (28%), 48 uro-gynecology (32%) and 40 oncologic gynecology (27%). Of all participating hematologists, 20 (32%) were employed at a hemophilia treatment center. 97% of gynecologists reported to manage HMB on a regular basis, compared to 60% of hematologists. In total 13% of respondents (28/211) participated in a multidisciplinary team discussion about bleeding disorders wherein HMB patients are discussed. This was more common among hematologists (34%) than gynecologists (5%).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eCharacteristics of respondents\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCharacteristics\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eGynecologists n\u0026thinsp;=\u0026thinsp;149\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eHematologists n\u0026thinsp;=\u0026thinsp;62\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eGynecologist\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e117 (78.5%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eResident gynecology\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e32 (21.5%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eGeneral internal medicine specialist\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e3 (4.8%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eInternist-hematologist\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e52 (83.9%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eInternist vascular medicine\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2 (3.2%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eResident internal medicine\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e5 (8.1%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHospital type\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eUniversity hospital\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e19 (12.8%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e18 (29.0%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eGeneral teaching hospital\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e88 (59.0%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e36 (58.1%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eGeneral non-teaching hospital\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e35 (23.5%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8 (12.9%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eIndependent treatment centre\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e7 (4.7%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0 (0%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFocussed HMB clinic present\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e30 (20.1%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e9 (14.5%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNo\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e119 (79.9%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e53 (85.5%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eStructured multidisciplinary team discussion regarding bleeding disorders and HMB\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e7 (4.7%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e21 (33.9%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNo\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e142 (95.3%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e41 (66.1%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e\n\u003ch3\u003eValues are n (%) \u003c/h3\u003e\n\u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eEstimated prevalence of underlying bleeding disorders in HMB\u003c/h2\u003e \u003cp\u003eThe estimates of the prevalence of bleeding disorders as the cause of HMB varied among respondents (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). Most respondents selected categories below the literature-based prevalence of 30% (8). The majority of gynecologists (89%) estimated a prevalence below 15%, with 40% placing it under 5%.\u003c/p\u003e \u003cp\u003eIn comparison, 63% of hematologists estimated the percentage to below 15%, and the majority of hematologists (77%) estimated it to be between 5\u0026ndash;30%. In respondents who have a focussed HMB clinic present (n\u0026thinsp;=\u0026thinsp;39), no difference was seen in the estimated prevalence of underlying bleeding disorders in HMB compared to those without such a clinic.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e \u003cem\u003e* Reported prevalence of underlying bleeding disorders in HMB according to the literature is 30% (8)\u003c/em\u003e \u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eDefinition HMB by hematologists\u003c/h3\u003e\n\u003cp\u003eIn order to assess which characteristics hematologists consider associated with HMB, and to explore the potential for alignment with gynecologists\u0026rsquo; definitions, hematologists were asked to select all relevant characteristics. Almost all symptoms were chosen in over 60% of the cases except for \u0026ldquo;losing clots\u0026rdquo; and \u0026ldquo;PBAC score\u0026thinsp;\u0026gt;\u0026thinsp;100\u0026rdquo; (Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eCharacteristics associated with HMB by hematologists\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"2\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHMB symptom\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eN\u0026thinsp;=\u0026thinsp;61\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMenstruation during \u0026gt;\u0026thinsp;7 days\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e43 (71%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eChanging pads more often than every two hours\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e54 (89%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLosing clots\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e26 (43%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePBAC score\u0026thinsp;\u0026gt;\u0026thinsp;100\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e24 (39%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eWork/school omission\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e46 (75%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHormonal therapy related to HMB\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e39 (64%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eIron deficiency anemia\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e39 (64%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNeed for iron supplementation\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e45 (72%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNeed for blood transfusion\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e57 (93%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e\u003cem\u003e Values are n (%), characteristics were based on HMB ACOG and NICE guidelines, as well as the ISTH-BAT questionnaire(15, 16)\u003c/em\u003e\u003c/p\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eScreening tool: pre-visit questionnaire\u003c/h2\u003e \u003cp\u003eTable\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e provides an overview of the pre-visit questionnaires used by gynecologist and hematologists (multiple options possible). The majority of respondents indicated that no questionnaires were send to patients prior to the consultation. Among gynecologists and hematologists, respectively 20% and 9% reported using any form of questionnaire. The \u0026lsquo;PBAC/menstruation calendar\u0026rdquo; and a \u0026lsquo;self-developed questionnaire\u0026rsquo; were most commonly used by gynecolgists. A \u0026lsquo;self-developed questionnaire\u0026rsquo; was not further defined.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eQuestionnaires before visit, multiple options possible\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eQuestionnaire\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eResponding gynecologists n\u0026thinsp;=\u0026thinsp;149\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eResponding hematologists n\u0026thinsp;=\u0026thinsp;58\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNo questionnaire\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e120 (80%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e53 (91%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eQuestionnaire\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e29 (20%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e5 (9%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePBAC/menstruation calendar\u003csup\u003e#\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e17 (11%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2 (3%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eISTH-BAT\u003csup\u003e#\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0 (0%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e4 (7%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSelf-BAT\u003csup\u003e#\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0 (0%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSelf-developed questionnaire\u003csup\u003e#\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e15 (10%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDifferent questionnaire*\u003csup\u003e#\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e6 (4%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2 (3%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eValues are n (%)\u003c/h3\u003e\n\u003cp\u003e \u003cem\u003ePBAC\u0026thinsp;=\u0026thinsp;Pictorial Blood Loss Assessment Chart, ISTH-BAT\u0026thinsp;=\u0026thinsp;International Society on Thrombosis and Hemostasis Bleeding Assessment Tool, Self-BAT\u0026thinsp;=\u0026thinsp;self Bleeding Assessment Tool\u003c/em\u003e \u003c/p\u003e \u003cp\u003e \u003cem\u003e*intake questionnaire, decision aid, uterine fibroid symptom and quality of life questionnaire or general hospital questionnaire.\u003c/em\u003e \u003c/p\u003e \u003cp\u003e \u003csup\u003e \u003cem\u003e#\u003c/em\u003e \u003c/sup\u003e \u003cem\u003eRespondents could give multiple answers\u003c/em\u003e\u003c/p\u003e\n\u003ch3\u003eScreening tool: anamnestic and laboratory evaluation\u003c/h3\u003e\n\u003cp\u003eWhile respondents working as gynecologists (n\u0026thinsp;=\u0026thinsp;149) did not routinely inquire about bleeding history or a family history of bleeding disorders, more than 80% (52/62 and 49/62) of hematologist respondents reported that they consistently ask about these aspects (Fig.\u0026nbsp;3). A bleeding score (ISTH BAT) is never used by 75% (112/149) of gynecologist respondents. Only 6% of gynecologists reported frequently using laboratory tests to detect bleeding disorders.\u003c/p\u003e \u003cp\u003e \u003cb\u003eFigure 3. Anamnestic and laboratory evaluation practices among gynecologists and hematologists\u003c/b\u003e \u003c/p\u003e \u003cp\u003e \u003cem\u003e*responding gynecologists n\u0026thinsp;=\u0026thinsp;149 for bleeding history, family history in the context of bleeding disorders, and bleeding score (ISTH BAT, n\u0026thinsp;=\u0026thinsp;145 for laboratory evaluation in the context of bleeding disorders. Responding hematologists n\u0026thinsp;=\u0026thinsp;62.\u003c/em\u003e \u003c/p\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eLaboratory testing in the context of bleeding disorders\u003c/h2\u003e \u003cp\u003eA total of 145 gynecologists responded to the question \u0026lsquo;which laboratory tests do you use in the first step? (multiple options possible)\u0026rsquo;. When performing laboratory testing, most gynecologists initially requested hemoglobin/hematocrit (132/145), ferritin (78/145) and von Willebrand activity (75/145). Common laboratory tests requested by hematologists are platelet count (62/62), hemoglobin/hematocrit (61/62), prothrombin time, activated partial thromboplastin time (60/62) and von Willebrand activity (51/62). Figure\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e4\u003c/span\u003e shows an overview of the laboratory tests performed.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e \u003cem\u003eHb/Ht\u0026thinsp;=\u0026thinsp;Hemoglobin(Hb)/Hematocrit, PT\u0026thinsp;=\u0026thinsp;Prothrombin time, APTT\u0026thinsp;=\u0026thinsp;Activated partial thromoplastin time, PFA\u0026thinsp;=\u0026thinsp;Platelet function assay\u003c/em\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eReferral to a hematologist\u003c/h2\u003e \u003cp\u003eOf 149 respondents who work as a gynecologist, 26 reported that they \u0026lsquo;never\u0026rsquo; refer patients with HMB to a hematologist, 114 gynecologists refer \u0026lsquo;seldom\u0026rsquo;, 7 refer \u0026lsquo;regularly\u0026rsquo; and 2 refer \u0026lsquo;often\u0026rsquo;. None of the responders reported to \u0026lsquo;always\u0026rsquo; refers patients. Figure\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e5\u003c/span\u003e provides an overview of all referral rates.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec13\" class=\"Section2\"\u003e \u003ch2\u003eGuideline HMB\u003c/h2\u003e \u003cp\u003e We finally analyzed whether gynecologists believe that the Dutch guideline for HMB (NVOG), gynecologists provide sufficient information on background and diagnostics of bleeding disorders as this may influence awareness and clinical practice. Of the respondents, 49% reported the information as insufficient.\u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cdiv id=\"Sec15\" class=\"Section2\"\u003e \u003ch2\u003eMain findings\u003c/h2\u003e \u003cp\u003eOur study evaluated the awareness and diagnostic work up regarding underlying bleeding disorders in patients with HMB among gynecologists and hematologists in the Netherlands. Both groups substantially underestimated the evidence-based prevalence of 30% (8), although hematologists provided estimates closer to the reported prevalence. Pre-visit questionnaires were rarely used, and gynecologists did not apply screening tools to identify an increased risk of an underlying bleeding disorder in HMB (i.e. BAT questionnaires) prior to consultation. During or after consultation, gynecologists scarcely applied anamnestic (e.g. the ISTH BAT) and laboratory evaluation aimed at identifying bleeding disorders. Moreover, 94% of responding gynecologists seldom or never refer HMB patients to a hematologist for further analysis, which aligns with their perception of low prevalence.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec16\" class=\"Section2\"\u003e \u003ch2\u003eInterpretation\u003c/h2\u003e \u003cp\u003eThe underestimation of the prevalence, low referral rate, and infrequent use of anamnestic and diagnostic evaluation among gynecologists demonstrates limited awareness or prioritization of bleeding disorders in the evaluation of HMB. Similarly, hematologists tend to underestimate the prevalence of bleeding disorders in HMB. Despite the need for effective multidisciplinary management of HMB (13, 17), only 13% of respondents participate in a multidisciplinary team discussion about bleeding disorders and HMB. Together this may lead to missed opportunities for timely diagnosis and treatment. Moreover, undiagnosed bleeding disorders can lead to inappropriate treatment, unnecessary procedures (endometrial ablation, hysterectomy), and preventable complications in trauma, surgery or childbirth (11, 12). The limited awareness may be partly attributable to the current Dutch HMB guideline, which according to 49% of responding gynecologists, provides limited guidance on how to screen for bleeding disorders. Its main focus is to screen for anatomical/structural disorders as a cause of HMB (14). The lack of clear guidelines may stem from the limited high-quality evidence on effective screening strategies available to gynecologists. We moreover found that multidisciplinary team meetings on bleeding disorders and HMB are uncommon in the Netherlands, which may further contribute to low awareness, and limited referrals and diagnostic evaluation. This warrants attention as Curry \u003cem\u003eet al.\u003c/em\u003e demonstrated that 90% of women with inherited bleeding disorders consider a multidisciplinary model as beneficial (17). Similarly, van Galen \u003cem\u003eet al.\u003c/em\u003e conclude the need for effective multidisciplinary management of HMB in bleeding disorders (13).\u003c/p\u003e \u003cp\u003eHematologists also underestimate the prevalence of bleeding disorders in women with HMB, and show gaps in recognizing symptoms that indicate HMB. This may partly explain previous findings that HMB is underestimated in hemophilia treatment centers (13). Aligning definitions between hematologists and gynecologists may support more consistent interpretation and communication in multidisciplinary settings, even though we found that multidisciplinary discussions on HMB and bleeding disorders are not routinely implemented. Pre-visit questionnaires are scarcely used by hematologists and the self-BAT is never applied despite validation studies (18). Hematologists however, frequently use the ISTH-BAT during consultations. Notably, 7% of hematologist respondents send this questionnaire to their patients prior to consultation despite it is designed as a physician-administered questionnaire.\u003c/p\u003e \u003cp\u003eOur study demonstrates that awareness has remained largely unchanged over the past two decades. Surveys among gynecologists in the US (2002) and UK (2006) revealed that bleeding disorders were considered rare causes of HMB, with only 4% of US respondents considering von Willebrand disease (7) and most UK respondents estimating its prevalence at \u0026lt;\u0026thinsp;1% (19). Indeed, women with bleeding disorders remain underrecognized and underdiagnosed worldwide, reflecting longstanding gender bias in care (20). This underdiagnosis may be partly due to a lack of consensus who to screen for bleeding disorders in HMB. Our findings indicate that screening tools to identify HMB patients suspected of having a bleeding disorder are hardly used. Even when a gynecological cause for HMB is identified, clinicians should consider the possibility of a coexisting bleeding disorder, as these conditions are not mutually exclusive (21). Several international guidelines recommend screening individuals presenting with HMB for a potential bleeding disorder. However, these guidelines lack consistency in their recommendations. The American College of Obstetricians and Gynecologists (ACOG) offers a committee opinion (2019) on screening HMB adolescents (15). They recommend to identify risk factors for bleeding disorders when obtaining a medical history, and suggest using the adapted Philipp screening tool (2011) (22). The National Institute for Health and Care Excellence (NICE) recommends to consider testing for bleeding disorders in women who present with HMB since menarche, and having a personal or family history suggesting a bleeding disorder (6). In our study, 30% of responding gynecologists reported routinely assessing a personal bleeding history, whereas 40% indicated that they rarely inquire about a family history suggestive for a bleeding disorder. The NVOG currently advises against routine screening for von Willebrand disease in cases of HMB, and provides no further guidance on how to screen for bleeding disorders in this context (14).\u003c/p\u003e \u003cp\u003eConsequently, it is not surprising that laboratory testing to detect bleeding disorders is rarely used by gynecologists in HMB patients. In our survey, only 6% of gynecologist respondents indicated that they often use laboratory testing for bleeding disorders. Comprehensive coagulation tests are moreover not routinely available in general hospitals in the Netherlands. Combined with limited awareness and weak collaboration with hematology department, this likely explains the limited laboratory evaluation observed. Previous studies confirm limited laboratory testing. An Australian retrospective audit showed that 40\u0026ndash;54% of women with HMB who attended a tertiary women\u0026rsquo;s hospital and were at risk of having a mild bleeding disorder were not tested for (23). In post-pubertal girls and adolescents with HMB, von Willebrand disease screening occurred in only 8% of cases and 16% of severe (24). Similarly, a UK survey reported that just 12% of gynecologists would arrange testing an 18-year-old with HMB for von Willebrand disease, and only 2% would test a 35-year-old [16]. In our study, 94% of responding gynecologists rarely or never referred to a hematologist for further evaluation of the coagulation system. This is in line with the study of Dilley \u003cem\u003eet al.\u003c/em\u003e in 2002 who demonstrated that only 3% of surveyed American gynecologists refer HMB patients to other specialists (7). The persistence of such low referral rates over decades suggests systemic gaps in interdisciplinary collaboration.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec17\" class=\"Section2\"\u003e \u003ch2\u003eStrengths \u0026amp; limitations\u003c/h2\u003e \u003cp\u003eA major strength of this study is the nationwide scope, including both gynecologists and hematologists, providing complementary perspectives on the diagnostic approach to bleeding disorders in HMB patients. Moreover, the survey addressed not only perceived prevalence but also evaluation and referral practices, highlighting awareness and practice gaps as key targets for improving care pathways. Additionally, the survey is developed and refined in collaboration with an expert group, which ensured that the questions were clearly formulated and that the response options closely reflected daily practice. Several limitations should be acknowledged. First, due to anonymity, center-level comparisons could not be made, and findings are based on self-reported practices rather than observed behavior. Second, volunteer bias may have influenced the results. Physicians with a particular interest or involvement in this subject are likely overrepresented in the sample, which may limit the representativeness of Dutch gynecologists and hematologists managing HMB. These respondents may have been more knowledgeable or attentive in completing the questionnaire, potentially leading to an overestimation of best practices. Finally, of all notified practitioners, only 9.8% of gynecologists and 9.5% of hematologists in the Netherlands were included.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec18\" class=\"Section2\"\u003e \u003ch2\u003eFuture studies\u003c/h2\u003e \u003cp\u003eFuture studies should focus on strategies to increase awareness of bleeding disorders as an underlying cause of HMB, as this is essential for appropriate referral and a timely diagnosis. In addition, research is essential to develop and validate efficient, practical screening tools that can be implemented in gynecology practice. These tools should aim to identify women with HMB at risk for bleeding disorders early in the diagnostic process. Finally, the development of a uniform international guideline for the assessment of bleeding disorders in HMB is warranted to reduce diagnostic delays, and improve diagnostic work-up and appropriate patient care.\u003c/p\u003e \u003c/div\u003e"},{"header":"Conclusion","content":"\u003cp\u003eOur study demonstrates that awareness of underlying bleeding disorders in women with HMB has remained largely unchanged over the past two decades. The prevalence is underestimated, particularly by gynecologists but also by hematologists, and referral rates remain low. Diagnostic work-up, including screening tools and laboratory testing is not routinely used by gynecologists, and structured multidisciplinary discussions are lacking in both specialities. These findings highlights the need for clearer guidelines, targeted education, practical screening tools, and stronger collaboration between gynecology and hematology.\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003cdiv class=\"DefinitionList\"\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eHMB\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eheavy menstrual bleeding\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eFIGO\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eFederation of Gynecology and Obstetrics\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eNVOG\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eDutch Society of Obstetrics and Gynecology\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eMMC\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eM\u0026aacute;xima Medical Center\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eWMO\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eMedical Research Involving Human Subjects Act\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eNVVH\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eDutch Association for Hematologists\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eISTH BAT\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eInternational Society on Thrombosis and Hemostasis Bleeding Assessment Tool\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eSPSS\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eStatistical Packages for Social Sciences\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eIBM\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eInternational Business Machines Corporation\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eACOG\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eAmerican College of Obstetricians and Gynecologists\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv class=\"DefinitionListEntry\"\u003e \u003cdiv class=\"Term\"\u003eNICE\u003c/div\u003e \u003cdiv class=\"Description\"\u003e \u003cp\u003eNational Institute for Health and Care Excellence\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003c/div\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cem\u003eEthics approval and consent to participate\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eThe Local Feasibility Research Committee at MMC granted feasibility approval (2023-MMC-056). This study involved an anonymous, voluntary online survey distributed to all gynecologists and hematologists in the Netherlands. Participation required respondents to actively open the survey link and complete the questionnaire. According to our Medical Ethics Committee (M\u0026aacute;xima Medical Centre), the study did not fall under the Medical Research Involving Human Subjects Act (WMO), and written informed consent was therefore not required. Completion and submission of the anonymous questionnaire were considered to imply informed consent. Respondents were informed in the invitation email and at the start of the survey about the study purpose, voluntary participation, anonymity, and data handling. No identifiable personal data were collected.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eConsent for publication\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eAvailability of data and materials\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eThe datasets used and analyzed during the current study available from the corresponding author on reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eCompeting interests\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare that they have no financial interests or personal relationships that could have appeared to influence the work of this paper.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eFunding\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eAuthor\u0026rsquo;s contributions\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eS.L., L.N., M.Y.B., J.C.L. and P.M.A.J.G., conceptualized the study;\u003c/p\u003e\n\u003cp\u003eS.L. was responsible for date collection;\u003c/p\u003e\n\u003cp\u003eS.L. drafted the manuscript;\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eS.G., L.N., M.Y.B., J.C.L., P.M.A.J.G. revised it critically for important intellectual content.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eAll authors read and approved the final manuscript.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eFraser IS, Mansour D, Breymann C, et al. Prevalence of heavy menstrual bleeding and experiences of affected women in a European patient survey. International Journal of Gynaecology and Obstetrics: The Official Organ of the International Federation of Gynaecology and Obstetrics. 2015;128(3):196-200.\u003c/li\u003e\n\u003cli\u003eAkiyama S, Tanaka E, Cristeau O, et al. Treatment patterns and healthcare resource utilization and costs in heavy menstrual bleeding: a Japanese claims database analysis. J Med Econ. 2018;21(9):853-860.\u003c/li\u003e\n\u003cli\u003eSchoep ME, Adang EMM, Maas JWM, et al. Productivity loss due to menstruation-related symptoms: a nationwide cross-sectional survey among 32 748 women. BMJ open. 2019;Jun 27;9(6):e026186(2044-6055 (Electronic)).\u003c/li\u003e\n\u003cli\u003eMunro MG, Critchley HOD, Fraser IS, Committee FMD. The two FIGO systems for normal and abnormal uterine bleeding symptoms and classification of causes of abnormal uterine bleeding in the reproductive years: 2018 revisions. International journal of gynaecology and obstetrics: the official organ of the International Federation of Gynaecology and Obstetrics. 2018;143(3):393-408.\u003c/li\u003e\n\u003cli\u003eMunro MG, Critchley HOD, Broder MS, Fraser IS. FIGO classification system (PALM-COEIN) for causes of abnormal uterine bleeding in nongravid women of reproductive age. International Journal of Gynaecology and Obstetrics: The Official Organ of the International Federation of Gynaecology and Obstetrics. 2011;113(1):3-13.\u003c/li\u003e\n\u003cli\u003eHeavy menstrual bleeding: assessment and management NICE guideline. 2018.\u003c/li\u003e\n\u003cli\u003eDilley A, Drews C, Lally C, et al. A survey of gynecologists concerning menorrhagia: perceptions of bleeding disorders as a possible cause. J Womens Health Gend Based Med. 2002;11(1):39-44.\u003c/li\u003e\n\u003cli\u003eComishen KJ, Bhatt M, Yeung K, et al. Etiology and diagnosis of heavy menstrual bleeding among adolescent and adult patients: a systematic review and meta-analysis of the literature. J Thromb Haemost. 2025;23(3):863-876.\u003c/li\u003e\n\u003cli\u003eHall EM, Ravelo AE, Aronoff SC, Del Vecchio MT. Systematic review and meta-analysis of the etiology of heavy menstrual bleeding in 2,770 adolescent females. BMC Womens Health. 2024;24(1):136.\u003c/li\u003e\n\u003cli\u003eShankar M, Lee CA, Sabin CA, et al. von Willebrand disease in women with menorrhagia: a systematic review. BJOG. 2004;111(7):734-740.\u003c/li\u003e\n\u003cli\u003eKulkarni R. Improving care and treatment options for women and girls with bleeding disorders. Eur J Haematol. 2015;Dec:95 Suppl 81:2-10(1600-0609 (Electronic)).\u003c/li\u003e\n\u003cli\u003eSanigorska AA-O, Chaplin SA-O, Holland MA-O, et al. The lived experience of women with a bleeding disorder: A systematic review. Research and practice in thrombosis and haemostasis. 2022(2475-0379 (Electronic)).\u003c/li\u003e\n\u003cli\u003eGalen KPM, Lavin M, Skouw‐rasmussen N, et al. Clinical management of woman with bleeding disorders: A survey among European haemophilia treatment centres. Wiley; 2020. p. 657.\u003c/li\u003e\n\u003cli\u003eSpecialisten FM. Guideline Heavy Menstrual Bleeding (HMB) Kennisinstituut van de Federatie van Medisch Specialisten DSoOa. 2012-2024.\u003c/li\u003e\n\u003cli\u003eOpninion AC. Screening and Management of Bleeding Disorders in Adolescents With Heavy Menstrual Bleeding. American College of Obstretricians and Gynecologists. 2019;134: e-71-83.\u003c/li\u003e\n\u003cli\u003eNice Clinical Guidelines N. Heavy Menstrual Bleeding. London: RCOG Press; 2018. Contract No.: Report.\u003c/li\u003e\n\u003cli\u003eCurry N, Bowles L, Clark TJ, et al. Gynaecological management of women with inherited bleeding disorders. A UK Haemophilia Centres Doctors\u0026apos; Organisation Guideline. Wiley; 2022. p. 917.\u003c/li\u003e\n\u003cli\u003ePunt MC, Blaauwgeers MW, Timmer MA, et al. Reliability and Feasibility of the Self-Administered ISTH-Bleeding Assessment Tool. TH open : companion journal to thrombosis and haemostasis. 2019;3(4):e350-e355.\u003c/li\u003e\n\u003cli\u003eChi C, Shiltagh N, Kingman CEC, et al. Identification and management of women with inherited bleeding disorders: a survey of obstetricians and gynaecologists in the United Kingdom. Haemophilia: The Official Journal of the World Federation of Hemophilia. 2006;12(4):405-412.\u003c/li\u003e\n\u003cli\u003eWeyand AC, James PD. Sexism in the management of bleeding disorders. Research and Practice in Thrombosis and Haemostasis. 2021;5(1):51-54.\u003c/li\u003e\n\u003cli\u003eKnol HM, Mulder AB, Bogchelman DH, et al. The prevalence of underlying bleeding disorders in patients with heavy menstrual bleeding with and without gynecologic abnormalities. Am J Obstet Gynecol. 2013;209(3):202.e201-207.\u003c/li\u003e\n\u003cli\u003ePhilipp CS, Faiz A Fau - Heit JA, Heit Ja Fau - Kouides PA, et al. Evaluation of a screening tool for bleeding disorders in a US multisite cohort of women with menorrhagia. Am J Obstet Gynecol. 2011(1097-6868 (Electronic)).\u003c/li\u003e\n\u003cli\u003eDkeidek A, Mattinson R, Grover SR. Bleeding disorders: Are gynaecologists testing women at risk? Haemophilia: The Official Journal of the World Federation of Hemophilia. 2021;27(4):e534-e536.\u003c/li\u003e\n\u003cli\u003eJacobson AE, Vesely SK, Koch T, et al. Patterns of von Willebrand Disease Screening in Girls and Adolescents With Heavy Menstrual Bleeding. Obstet Gynecol. 2018;131(6):1121-1129.\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"bmc-womens-health","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bmwh","sideBox":"Learn more about [BMC Women's Health](http://bmcwomenshealth.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bmwh/default.aspx","title":"BMC Women's Health","twitterHandle":"","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"women’s health, heavy menstrual bleeding, bleeding disorders, awareness","lastPublishedDoi":"10.21203/rs.3.rs-8310699/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-8310699/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eBackground\u003c/h2\u003e \u003cp\u003eHeavy menstrual bleeding (HMB) is common in the general population, affecting at least one-quarter of women of reproductive age. A bleeding disorder has been reported as an underlying cause of HMB in 30% of hospital-seen cases suffering from HMB. Despite this, bleeding disorders appear to be substantially underdiagnosed in HMB. Our primary objective is to evaluate the awareness and diagnostic work up regarding bleeding disorders in patients with HMB among gynecologists and hematologists in the Netherlands.\u003c/p\u003e\u003ch2\u003eMethods\u003c/h2\u003e \u003cp\u003eAn online questionnaire was conducted in 2023. The survey was distributed by email, with an anonymous link to 1508 gynecologists and 646 hematologists.\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eOf the 2154 emails sent, 261 surveys were analyzed: 149 from gynecologists and 62 from hematologists representing a 10% response rate. Most gynecologists (89%) estimated the prevalence of bleeding disorders in HMB to be below 15%, with 40% under 5%. In comparison, the majority of hematologists (77%) placed their estimate between 5%-30%. Screening tools, including pre-visit questionnaires, anamnestic or laboratory evaluation, were not structurally used by gynecologists. Only 5% of gynecologists reported participating in multidisciplinary team meetings on bleeding disorders and HMB, compared to 34% of hematologists. Moreover, 94% of responding gynecologists reported seldom or never referring HMB patients to a hematologist.\u003c/p\u003e\u003ch2\u003eConclusions\u003c/h2\u003e \u003cp\u003eThis study highlights the underestimation of the prevalence of bleeding disorders among patients with HMB. Systematic screening for bleeding disorders in patients with HMB by gynecologists is largely lacking. These findings underscore the necessity of increasing awareness of bleeding disorders and to implement a structured diagnostic workup of HMB.\u003c/p\u003e","manuscriptTitle":"A persistent diagnostic gap: awareness and workup of bleeding disorders in heavy menstrual bleeding among Dutch gynecologists and hematologists","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2026-01-12 06:09:33","doi":"10.21203/rs.3.rs-8310699/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2026-01-27T21:40:29+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-01-23T18:17:56+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"8203916840577908343291810876329043266","date":"2026-01-21T06:05:51+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-01-18T15:49:11+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"297084540960078773168061389213607897067","date":"2026-01-18T15:27:08+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-01-18T02:13:20+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"285378973959479582669071656596671778942","date":"2026-01-14T12:05:59+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-01-14T07:48:21+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"5416447964320770041684795249786104209","date":"2026-01-14T07:14:42+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"99864236990703426639752864005337052152","date":"2026-01-09T20:53:45+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2026-01-07T10:14:09+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2025-12-15T16:23:49+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2025-12-11T23:52:57+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2025-12-11T23:52:33+00:00","index":"","fulltext":""},{"type":"submitted","content":"BMC Women's Health","date":"2025-12-08T19:25:47+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"bmc-womens-health","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bmwh","sideBox":"Learn more about [BMC Women's Health](http://bmcwomenshealth.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bmwh/default.aspx","title":"BMC Women's Health","twitterHandle":"","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"ad58ab12-27f3-4123-9fa4-766b908bbc0f","owner":[],"postedDate":"January 12th, 2026","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2026-04-13T16:15:27+00:00","versionOfRecord":{"articleIdentity":"rs-8310699","link":"https://doi.org/10.1186/s12905-026-04444-9","journal":{"identity":"bmc-womens-health","isVorOnly":false,"title":"BMC Women's Health"},"publishedOn":"2026-04-06 15:58:05","publishedOnDateReadable":"April 6th, 2026"},"versionCreatedAt":"2026-01-12 06:09:33","video":"","vorDoi":"10.1186/s12905-026-04444-9","vorDoiUrl":"https://doi.org/10.1186/s12905-026-04444-9","workflowStages":[]},"version":"v1","identity":"rs-8310699","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-8310699","identity":"rs-8310699","version":["v1"]},"buildId":"XKTyCvWXoU3ODBz1xrDgd","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}