Ackerman, Kathryn E

Adams, William M

Anderson, Travis

Casey, Ellen

Donaldson, Amber T

Elliott-Sale, Kirsty J

Finnoff, Jonathan T

Kraus, Emily

Oleka, Chimsom T

Post, Eric G

Stellingwerff, Trent

English

E-space: Manchester Metropolitan University's Research Repository

Please cite the Published VersionOleka, Chimsom T, Anderson, Travis , Ackerman, Kathryn E , Elliott-Sale, Kirsty J , Kraus,Emily , Casey, Ellen , Stellingwerff, Trent , Donaldson, Amber T, Finnoff, Jonathan T, Post,Eric G and Adams, William M (2024) An update to terminology describing abnormal uterinebleeding in female athletes: facilitating cross-disciplinary health care. British Journal of SportsMedicine. ISSN 0306-3674DOI: https://doi.org/10.1136/bjsports-2024-108261Publisher: BMJVersion: Accepted VersionDownloaded from: https://e-space.mmu.ac.uk/635819/Usage rights: In CopyrightAdditional Information: This article has been accepted for publication in British Journal of SportsMedicine, 2024, following peer review, and the Version of Record can be accessed online athttp://dx.doi.org/10.1136/bjsports-2024-108261 c© Authors (or their employer(s)).Enquiries:If you have questions about this document, contact openresearch@mmu.ac.uk. Please in-clude the URL of the record in e-space. If you believe that your, or a third party’s rights havebeen compromised through this document please see our Take Down policy (available fromhttps://www.mmu.ac.uk/library/using-the-library/policies-and-guidelines)1  Editorial Title: An Update to Terminology Describing Abnormal Uterine Bleeding in Female Athletes: 1 Facilitating Cross-Disciplinary Health Care 2 Authors: Chimsom T. Oleka1,13, Travis Anderson2,3, Kathryn E. Ackerman4,13, Kirsty J. Elliott-Sale6, 3 Emily Kraus5,13, Ellen Casey7,13, Trent Stellingwerff8,9,  Amber T. Donaldson2,3,13, Jonathan T. 4 Finnoff2,3,10, Eric G. Post2,3, William M. Adams2,3,11,12 5  6 1Department of Obstetrics and Gynecology, INOVA Fairfax Hospital, Falls Church, VA, USA 7 2Department of Sports Medicine, United States Olympic & Paralympic Committee, Colorado Springs, 8 CO, USA 9 3United States Coalition for the Prevention of Illness and Injury in Sport, Colorado Springs, CO, USA 10 4Wu Tsai Female Athlete Program, Boston Children’s Hospital; Neuroendocrine Unit, Massachusetts 11 General Hospital, Harvard Medical School, Boston, MA, USA 12 5Stanford Female Athlete Science and Translational Research (FASTR) Program, Department of 13 Orthopaedic Surgery, Stanford, CA, USA 14 6Department of Sport and Exercise Sciences, Manchester Metropolitan University Institute of Sport, 15 Manchester, UK 16 7Hospital for Special Surgery, New York, NY, USA 17 8Canadian Sport Institute - Pacific, Victoria, British Columbia, Canada 18 9Exercise Science, Physical & Health Education, University of Victoria, British Columbia, Canada 19 10Department of Physical Medicine and Rehabilitation, University of Colorado School of Medicine, 20 Denver, CO, USA 21 11Department of Kinesiology, University of North Carolina at Greensboro, Greensboro, NC, USA 22 12School of Health, Exercise and Sport Sciences, Loughborough University, Leicestershire, UK 23 13United States Olympic and Paralympic Committee Women’s Health Task Force, Colorado Springs, CO 24  25 Corresponding Author: Chimsom T. Oleka, MD, FACOG Division of Pediatric and Adolescent 26 Gynecology, Department of Obstetrics & Gynecology  INOVA Fairfax Hospital, 3300 Gallows Road, 27 Falls Church, VA 22042, USA 28 email: chimsom.oleka@inova.org  29  30 Acknowledgments: This work is the author’s own and not that of the United States Olympic & 31 Paralympic Committee or any of its members or affiliates. 32 Text Word Count: 978 33 Tables (#): 1 34 Figures (#): 0 35 References (#): 7  36 2  Female athlete health, performance, and well-being are best supported by a comprehensive team 37 of medical providers and sports scientists that may include physicians from various specialties, allied 38 health providers, exercise and sports scientists, mental health professionals, and dietitians. Understanding 39 and consistently utilizing contemporary terminology in research and clinical practice is critical to ensure 40 precise communication and facilitate effective cross-disciplinary health care. This editorial aims to 41 highlight current standardized terminology for describing abnormal menstrual bleeding in order to 42 promote consistency in terminology across sports and exercise science and medicine (SESM). 43 While there has been a recent increase in female athlete research, including studies investigating 44 the influence of the menstrual cycle on athletic performance and health (1), there is a clear absence of 45 standardized menstrual cycle language and classification due to the persistent use of outdated abnormal 46 uterine bleeding (AUB) nomenclature. Indeed, previous research and clinical investigation and 47 management of AUB among non-pregnant women of reproductive age was hindered by inconsistently 48 applied nomenclature and lack of standardized categorization of potential etiologies (2–5). This ambiguity 49 poses several problems, including the inability to homogenously classify research participants 50 experiencing AUB, difficulty comparing studies, and significantly undermining the investigative leverage 51 of meta-analyses due to increased risk of inaccurate conclusions, as well as clinical implications (e.g., 52 ambiguous diagnoses, less precise clinical care and management, and confusing communication across 53 the medical team). Such concerns led to the development of a universally accepted nomenclature and 54 classification system within the gynecological and obstetrics medical field ~20 years ago that is practical 55 and appropriate for research, education, and clinical needs. However, within the past 10 years, 56 publications across various medical and applied and basic science journals from fields such as sports 57 medicine, psychology, public health, and others have used outdated terms with little adoption of updated 58 language.  59 Abnormal Uterine Bleeding (AUB) Nomenclature 60 Recognizing the international need for AUB classification harmonization, the International 61 Federation of Gynecology and Obstetrics (FIGO) developed a system to define normal and abnormal 62 bleeding symptoms. It recommended classifications for the causes of AUB, reaching international 63 consensus in 2011 and updating in 2018 to facilitate research, education, and clinical care (6,7). This 64 terminology has been helpful in evolving collaborative research and applying evidence-based results to 65 clinical practice (6).  Readers are directed to Figure 1 in Munro et al. (7) for such definitions. Several key 66 points from the classification system are highly relevant to sports medicine clinicians and SESM 67 researchers. 68 Firstly, AUB was deemed a suitable overarching term for the symptom of disturbed menstrual 69 bleeding, not restricted to just abnormally heavy menstrual bleeding but including bleeding that was 70 abnormal in timing. The previous terminology was either discarded or replaced with the recognition of 71 3  disparate usage and inconsistent meaning for the clinical, academic, and general communities (6). See 72 Table 1 for updated terminology and definitions. 73  74 INSERT TABLE 1 ABOUT HERE 75  76 Secondly, the following general sources of bleeding were considered in the approved FIGO 77 classification system: 1) Primary disorders of the endometrium that most often manifest as disturbances 78 of local endometrial hemostasis but may also include other entities such as altered vasculogenesis or local 79 inflammatory response abnormalities; 2) Endometrial polyps; 3) Leiomyomas (fibroids); 4) 80 Adenomyosis; 5) Disorders of ovulatory function; 6) Systemic disorders of hemostasis known as 81 coagulopathies; 7) Malignant and premalignant conditions; 8) Iatrogenic causes including gonadal steroid 82 administration; 9) Other local lesions or systemic conditions that may be rare causes of AUB (e.g., 83 arteriovenous malformations and myometrial hypertrophy) or those that can sometimes cause abnormal 84 bleeding (e.g., endometriosis). Importantly, these FIGO classification systems relate solely to assessing 85 and managing non-gestational AUB. In addition, there are other causes of genital, urinary, or 86 gastrointestinal tract bleeding that do not originate from the uterus (6). 87 It was envisioned that the most straightforward components of the classification system would be 88 used in primary medical care, and sub-classifications would be most relevant in specialist clinical and 89 research settings.(6) The classification system of AUB causes in the reproductive years is comprised of 90 nine main categories that are arranged according to the acronym PALM-COEIN (pronounced “pahm-91 koin”): polyp; adenomyosis; leiomyoma; malignancy and hyperplasia (PALM); coagulopathy; ovulatory 92 dysfunction; endometrial; iatrogenic; and not otherwise classified (COEIN). Generally, the PALM group 93 consists of discrete (structural) components that can be visually measured using imaging techniques or 94 histopathology (6). In contrast, the COEIN group is associated with entities not characterized by imaging 95 or histopathology, falling into the non-structural category (6). The system was constructed with the 96 understanding that there could be one or more contributors to the presenting AUB. 97 Relevance of Standardized Terminology for Sports and Exercise Science and Medicine 98 We posit that using standardized terminology for abnormal menstrual bleeding is crucial in 99 SESM to enhance cross-disciplinary communication and care. This would benefit female athletes by 100 ensuring precise diagnoses and better management through a collaborative healthcare team. We also 101 believe that adopting the FIGO classification system for AUB in SESM research may potentially improve 102 consistency and comparison across studies, enable the collection of common data elements, and advance 103 scientific understanding and collaboration, ultimately leading to improved athlete health and performance. 104 Although efforts are being made, unfortunately, this change in terminology has not yet permeated 105 the SESM literature (1,8,9). Thus, researchers and clinicians outside of Obstetrics and Gynecology tend to 106 4  use previously accepted language when describing menstrual cycle disturbances (e.g., oligomenorrhea). If 107 researchers wish to enhance further cross-discipline collaboration, readership, and application of their 108 work related to menstrual cycle health, we suggest including the PALM-COEIN categorization (e.g., 109 abnormal uterine bleeding with ovulatory dysfunction or AUB-O; Table 1) in addition to more familiar 110 terminology that would otherwise be used. Future consensus statements on female athlete health and well-111 being may also consider adopting this classification system when reporting AUB. We, therefore, 112 encourage all sports medicine providers to become familiar with these terms to better facilitate athlete 113 screening, improve appropriate referrals to gynecology, and enhance overall female athlete care via cross-114 discipline collaboration and communication.  115  116 Statements 117 Equity, Diversity, and Inclusion Statement: The authors of this editorial represent a diverse genders, 118 countries, ethnicities, and sports medicine and sports science disciplines. 119 Conflict of Interest Statement: KEA receives research funding from the Joe and Clara Tsai Foundation as 120 part of the Wu Tsai Human Performance Alliance and from Nike. She receives speaker and writer 121 honoraria from Gatorade Sports Science Institute, Hologic, Springer, and UptoDate. She is a deputy editor 122 of the British Journal of Sports Medicine and an associate editor of the British Journal of Sports 123 Medicine’s Injury Prevention and Health Protection Edition. KJE-S has received funding/honoraria from 124 Arsenal Football Club, The UK Sports Institute, the European Club Association, Gatorade Sport Science 125 Institute, Hologic, Science in Sport, and the UK Ministry of Defence to support female athletes. TS has 126 received funding/honoraria from the Wu Tsai Human Performance Alliance, Ineos, Science in Sport (Sis) 127 Own The Podium, Gatorade Sport Science Institute and Lululemon Athletica to support research, 128 including projects on female participants. JTF receives royalties from UptoDate and Demos Publishing. 129 WMA serves on the advisory board for My Normative, where he receives stock options as compensation 130 for his efforts. WMA is a member of the Sport Advisory Council for the Wu Tsai Human Performance 131 Alliance. WMA also receives royalties from Springer Nature. EK receives research funding from the Joe 132 and Clara Tsai Foundation as part of the Wu Tsai Human Performance Alliance. None of the above 133 honoraria and funds have a direct competing interest with the content of this editorial. OTC, TA, EC, 134 ATD, EGP, and EC have nothing to disclose. 135 Contributorship: CTO was responsible for the initial draft of this editorial. TA was responsible for the 136 editorial conceptualization. All authors were responsible for the editorial critical review, editing, and 137 approval. Guarantor is CTO. 138 Acknowledgments: This work is the authors’ own and not that of the United States Olympic & Paralympic 139 Committee or any of its members or affiliates. 140 Funding: The authors have not declared a specific grant for this research from any funding agency in the 141 public, commercial or non-profit sectors  142 5  Ethical approval: Not required. 143 Data Sharing: No data to share. 144 Provenance and Peer Review: Not commissioned; externally peer-reviewed. 145 Patient Involvement: Patients were not involved in this editorial.  146   147 6  Tables 148 Table 1. Sports Medicine Relevant Changes to Abnormal Uterine Bleeding Terminology 149 Previous Terminology Action Replacement Terminology Description Amenorrhea Retained - Primary Amenorrhea: Failure of onset of menstruation by the age of 15 years. Evaluations for primary amenorrhea should also occur after age 14 without secondary sex characteristics or if there is no menarche 3 years after the onset of secondary sex characteristics. Secondary Amenorrhea: Absence of menstrual periods for more than 3-6 months^ in an individual who has had at least one spontaneous menses.  Luteal Phase Defect Specified AUB-E Abnormal bleeding due to inadequate levels of progesterone secretion. Anovulation (without amenorrhea) Specified AUB-O Abnormal uterine bleeding due to ovulatory dysfunction. Menorrhagia Replaced Heavy Menstrual Bleeding (HMB) Excessive bleeding from the uterine corpus that may interfere with the physical, emotional, social, and material qualities of life.  Metrorrhagia Replaced Intermenstrual Bleeding (IMB) Bleeding from the uterine corpus that occurs randomly or predictably outside of cyclic or scheduled menses. Dysfunctional menstrual bleeding Replaced Chronic AUB Bleeding from the uterine corpus that is abnormal in duration, volume, frequency, and/or regularity that has been present for greater than or equal to 6 months. Dysfunctional menstrual bleeding Replaced Acute AUB Abnormal, typically heavy, bleeding from the uterine corpus that requires immediate intervention to prevent further blood loss. Oligomenorrhea Replaced AUB-infrequent Menstrual cycle lengths more than 38 days. Polymenorrhea Replaced AUB-frequent Menstrual cycle lengths of fewer than 24 days. Dysfunctional uterine bleeding Discarded - - ^Munro et al. (10) specify 180 days. 150   151 7  References 152 1. Elliott-Sale KJ, Minahan CL, de Jonge XAJ, Ackerman KE, Sipilä S, Constantini NW, et al. 153 Methodological considerations for studies in sport and exercise science with women as participants: a 154 working guide for standards of practice for research on women. Sports Med. 2021;51(5):843–61.  155 2. Fraser IS, Critchley HO, Munro MG, Broder M. A process designed to lead to international agreement 156 on terminologies and definitions used to describe abnormalities of menstrual bleeding∗. Fertil Steril. 157 2007;87(3):466–76.  158 3. Fraser IS, Critchley HO, Munro MG. Abnormal uterine bleeding: getting our terminology straight. 159 Curr Opin Obstet Gynecol. 2007;19(6):591–5.  160 4. Fraser IS, Critchley H, Munro M, Broder M. Can we achieve international agreement on terminologies 161 and definitions used to describe abnormalities of menstrual bleeding? Hum Reprod. 2007;22(3):635–162 43.  163 5. Woolcock JG, Critchley HO, Munro MG, Broder MS, Fraser IS. Review of the confusion in current 164 and historical terminology and definitions for disturbances of menstrual bleeding. Fertil Steril. 165 2008;90(6):2269–80.  166 6. Munro MG, Critchley HO, Broder MS, Fraser IS, FIGO Working Group on Menstrual Disorders. 167 FIGO classification system (PALM-COEIN) for causes of abnormal uterine bleeding in nongravid 168 women of reproductive age. Int J Gynecol Obstet. 2011;113(1):3–13.  169 7. Munro MG, Critchley HO, Fraser IS, FIGO Menstrual Disorders Committee, Haththotuwa R, Kriplani 170 A, et al. The two FIGO systems for normal and abnormal uterine bleeding symptoms and classification 171 of causes of abnormal uterine bleeding in the reproductive years: 2018 revisions. Int J Gynecol Obstet. 172 2018;143(3):393–408.  173 8. Mountjoy M, Ackerman KE, Bailey DM, Burke LM, Constantini N, Hackney AC, et al. 2023 174 International Olympic Committee’s (IOC) consensus statement on relative energy deficiency in sport 175 (REDs). Br J Sports Med. 2023;57(17):1073–97.  176 9. Moore IS, Crossley KM, Bo K, Mountjoy M, Ackerman KE, da Silva Antero J, et al. Female athlete 177 health domains: a supplement to the International Olympic Committee consensus statement on 178 methods for recording and reporting epidemiological data on injury and illness in sport. Br J Sports 179 Med. 2023;57(18):1164–74.  180 10. Munro MG, Balen AH, Cho S, Critchley HO, Díaz I, Ferriani R, et al. The FIGO ovulatory disorders 181 classification system. Hum Reprod. 2022;37(10):2446–64.  182  183 

Editorial: An update to terminology describing abnormal uterine bleeding in female athletes: facilitating cross-disciplinary health care

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An update to terminology describing abnormal uterine bleeding in female athletes: facilitating cross-disciplinary health care

An update to terminology describing abnormal uterine bleeding in female athletes: facilitating cross-disciplinary health care

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