The Duration of Menstrual Blood Loss: Historical to Current Understanding
Abstract
:1. Introduction
2. Assessing the Duration of Bleeding
3. Identifying the Onset of Bleeding and Its Cessation
4. Assessing Variability
5. The Relation between the Amount of Loss and Its Duration
6. Factors That Affect the Duration of Bleeding
6.1. Mechanisms Involved in Menstruation
6.2. Endometrial Shedding and Its Anomalies
6.3. Triggering the Onset of Bleeding
6.4. The Lifespan of the Corpus Luteum
6.5. Factors That Affect Cessation of Bleeding
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Mena, G.P.; Mielke, G.I.; Brown, W.J. Prospective associations between physical activity and BMI with irregular periods and heavy menstrual bleeding in a large cohort of Australian women. Hum. Reprod. 2021, 36, 1481–1491. [Google Scholar] [CrossRef]
- Lebduska, E.; Beshear, D.; Spataro, B.M. Abnormal Uterine Bleeding. Med. Clin. N. Am. 2023, 107, 235–246. [Google Scholar] [CrossRef]
- Nazir, M.; Asghar, S.; Rathore, M.A.; Shahzad, A.; Shahid, A.; Ashraf Khan, A.; Malik, A.; Fakhar, T.; Kausar, H.; Malik, J. Menstrual abnormalities after COVID-19 vaccines: A systematic review. Vacunas 2022, 23, S77–S87. [Google Scholar] [CrossRef]
- Alahmadi, A.M.; Aljohani, A.H.; Fadhloun, R.A.; Almohammadi, A.S.; Alharbi, D.F.; Alrefai, L.S. The Effect of the COVID-19 Vaccine on the Menstrual Cycle among Reproductive-Aged Females in Saudi Arabia. Cureus 2022, 14, e32473. [Google Scholar] [CrossRef]
- Mínguez-Esteban, I.; García-Ginés, P.; Romero-Morales, C.; Abuín-Porras, V.; Navia, J.A.; Alonso-Pérez, J.L.; de la Cueva-Reguera, M. Association between RNAm-Based COVID-19 Vaccines and Permanency of Menstrual Cycle Alterations in Spanish Women: A Cross-Sectional Study. Biology 2022, 11, 1579. [Google Scholar] [CrossRef] [PubMed]
- Perelló-Capo, J.; Rius-Tarruella, J.; Andeyro-García, M.; Calaf-Alsina, J. Sensitivity to Change of the SAMANTA Questionnaire, a Heavy Menstrual Bleeding Diagnostic Tool, After 1 Year of Hormonal Treatment. J. Womens Health 2023, 32, 208–215. [Google Scholar] [CrossRef]
- Fraser, I.S.; Critchley, H.O.; Munro, M.G.; Broder, M. Can we achieve international agreement on terminologies and definitions used to describe abnormalities of menstrual bleeding? Hum. Reprod. 2007, 22, 635–643. [Google Scholar] [CrossRef]
- Munro, M.G.; Critchley, H.O.; Broder, M.S.; Fraser, I.S. FIGO Working Group on Menstrual Disorders. FIGO classification system (PALM-COEIN) for causes of abnormal uterine bleeding in nongravid women of reproductive age. Int. J. Gynecol. Obs. 2011, 113, 3–13. [Google Scholar] [CrossRef] [PubMed]
- Munro, M.G.; Critchley, H.O.D.; Fraser, I.S.; FIGO Menstrual Disorders Committee. 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. Int. J. Gynecol. Obs. 2018, 143, 393–408. [Google Scholar] [CrossRef] [PubMed]
- Bastianelli, C.; Grandi, G.; Farris, M.; Brandolino, G.; Paoni Saccone, G.; La Barbiera, I.; Benagiano, G. Attitudes towards menstruation: What women want? An Italian National Survey. Eur. J. Contracept. Reprod. Health Care 2023, 28, 28–35. [Google Scholar] [CrossRef]
- Eftekhar, T.; Ghaemi, M.; Abedi, A.; Shirazi, M. Comparison of misoprostol and mefenamic acid on reducing menstrual bleeding in patients suffering from heavy menstrual bleeding. J. Fam. Reprod. Health 2019, 13, 141–145. [Google Scholar] [CrossRef]
- Zhang, Q.; Wang, Y.; Zhang, Y.; Zhang, H.; Yang, Y.; He, Y.; Xu, J.H.; Zhao, J.; Peng, Z.Q.; Ma, X. The influence of age at menarche, menstrual cycle length and bleeding duration on time to pregnancy: A large prospective cohort study among rural Chinese women. BJOG 2017, 124, 1654–1662. [Google Scholar] [CrossRef] [PubMed]
- Meigs, C.D. The Physiology of Reproduction, in Obstetrics: The Science and the Art; Lea and Blanchard: Philadelphia, PA, USA, 1849; pp. 116–133. [Google Scholar]
- Tauszky, R. The Anomalies of Menstruation, Their Causes and Treatment. Lectures Delivered at the Mt. Sinai Hospital, Out-Door Department: New York, NY, USA, 1879. Available online: http://resource.nlm.nih.gov/101683193 (accessed on 20 March 2023).
- Snowden, R. The statistical analysis of menstrual bleeding patterns. J. Biosoc. Sci. 1977, 9, 107–120. [Google Scholar] [CrossRef]
- Belsey, E.M.; Carlson, N. The description of menstrual bleeding patterns: Towards fewer measures. Stat. Med. 1991, 10, 267–284. [Google Scholar] [CrossRef]
- Rodriguez, G.; Faundes-Latham, A.; Atkinson, L.E. An approach to the analysis of menstrual patterns in the critical evaluation of contraceptives. Stud. Fam. Plan. 1976, 7, 42–51. [Google Scholar] [CrossRef]
- Vollman, R.F. The Menstrual Cycle; WB Saunders: Philadelphia, PA, USA, 1977. [Google Scholar]
- McLennan, C.E.; Rydell, A.H. Extent of endometrial shedding during normal menstruation. Obs. Gynecol. 1965, 26, 605–621. [Google Scholar]
- Li, K.; Urteaga, I.; Wiggins, C.H.; Druet, A.; Shea, A.; Vitzthum, V.J.; Elhadad, N. Characterizing physiological and symptomatic variation in menstrual cycles using self-tracked mobile-health data. Npj Digit. Med. 2020, 3, 79. [Google Scholar] [CrossRef] [PubMed]
- Bull, J.R.; Rowland, S.P.; Scherwitzl, E.B.; Scherwitz, I.R.; Danielsson, K.G.; Harper, J. Real-world menstrual cycle characteristics of more than 600,000 menstrual cycles. Npj Digit. Med. 2019, 2, 83. [Google Scholar] [CrossRef]
- Dallenbach-Hellweg, G. Histopathology of the Endometrium; Springer: Berlin/Heidelberg, Germany, 1987. [Google Scholar]
- Bengtsson, L.P.; Ingemansson, C.A. Amenorrhoea associated with retention of fertility. Acta Obs. Gynecol. Scand. 1959, 38, 62–67. [Google Scholar] [CrossRef]
- Philippe, E.; Ritter, J.; Gandar, R. L’endomètre biphasique normal en période menstruelle [The normal biphasic endometrium in the menstrual period]. Gynecol. Obstet. 1966, 65, 515–531. [Google Scholar]
- Belsey, E.M.; Farley, T.M.M. The analysis of menstrual bleeding patterns: A review. Appl. Stoch. Models Data Anal. 1987, 3, 125–150, Reprinted Contraception 1988, 38, 129–156. [Google Scholar] [CrossRef] [PubMed]
- Donald, J.L.; Fraser, I.S.; Duncan, L.; McCarron, G. Analysis of the time of day of onset of menstruation. Clin. Reprod. Fertil. 1987, 5, 77–83. [Google Scholar] [PubMed]
- Goldzieher, J.W.; Henkins, A.E.; Hamblen, E.C. Characteristics of normal menstrual cycle. Am. J. Obs. Gynecol. 1947, 54, 668–675. [Google Scholar] [CrossRef] [PubMed]
- Najmabadi, S.; Schliep, K.C.; Simonsen, S.E.; Porucznik, C.A.; Egger, M.J.; Stanford, J.B. Menstrual bleeding, cycle length, and follicular and luteal phase lengths in women without known subfertility: A pooled analysis of three cohorts. Paediatr. Perinat. Epidemiol. 2020, 34, 318–327. [Google Scholar] [CrossRef]
- Belsey, E.M.; Pinol, A.P. Menstrual bleeding patterns in untreated women. Task Force on Long-Acting Systemic Agents for Fertility Regulation. Contraception 1997, 55, 57–65. [Google Scholar] [CrossRef] [PubMed]
- Treloar, A.E.; Boynton, R.E.; Behn, B.G.; Brown, B.W. Variation of the human menstrua] cycle through reproductive life. Int. J. Fertil. 1967, 12, 77–126. [Google Scholar]
- Chiazze, L.; Brayer, F.T.; Macisco, J.J.; Parker, M.P.; Duffy, B.J. The length and variability of the human menstrual cycle. JAMA 1968, 203, 89–92. [Google Scholar] [CrossRef]
- World Health Organization. Task force on methods for the determination of the fertile period. A prospective multicentre trial of the ovulation method of natural family planning. III. Characteristics of the menstrual cycle and of the fertile phase. Fertil. Steril. 1983, 40, 773–778. [Google Scholar] [CrossRef]
- Harlow, S.D.; Zeger, S.L. An application of longitudinal methods to the analysis of menstrual diary data. J. Clin. Epidemiol. 1991, 44, 1015–1025. [Google Scholar] [CrossRef]
- Habiba, M.A.; Bell, S.C.; Abrams, K.; al-Azzawi, F. Endometrial responses to hormone replacement therapy: The bleeding pattern. Hum. Reprod. 1996, 11, 503–508. [Google Scholar] [CrossRef]
- Rybo, G. Menstrual blood loss in relation to parity and menstrual pattern. Acta Obs. Gynecol. Scand. 1966, 45 (Suppl. S7), 25–45. [Google Scholar] [CrossRef]
- Barer, A.P.; Fowler, W.M. The blood loss during normal menstruation. Am. J. Obs. Gynecol. 1936, 31, 979–986. [Google Scholar] [CrossRef]
- Haynes, P.J.; Hodgson, H.; Anderson, A.B.; Turnbull, A.C. Measurement of menstrual blood loss in patients complaining of menorrhagia. Br. J. Obs. Gynecol. 1977, 84, 763–768. [Google Scholar] [CrossRef] [PubMed]
- Chimbira, T.H.; Anderson, A.B.; Turnbull, A.C. Relation between measured menstrual blood loss and patient’s subjective assessment of loss, duration of bleeding, number of sanitary towels used, uterine weight and endometrial surface area. Br. J. Obs. Gynecol. 1980, 87, 603–609. [Google Scholar] [CrossRef]
- Hytten, F.E.; Cheyne, G.A.; Klopper, A.I. Iron loss at menstruation. J Obs. Gynecol. Br. Commonw. 1964, 71, 255–259. [Google Scholar] [CrossRef] [PubMed]
- Kadir, R.A.; Economides, D.L.; Sabin, C.A.; Pollard, D.; Lee, C.A. Assessment of menstrual blood loss and gynaecological problems in patients with inherited bleeding disorders. Haemophilia 1999, 5, 40–48. [Google Scholar] [CrossRef]
- Dasharathy, S.S.; Mumford, S.L.; Pollack, A.Z.; Perkins, N.J.; Mattison, D.R.; Wactawski-Wende, J.; Schisterman, E.F. Menstrual bleeding patterns among regularly menstruating women. Am. J. Epidemiol. 2012, 175, 536–545. [Google Scholar] [CrossRef]
- Najmabadi, S.; Schliep, K.C.; Simonsen, S.E.; Porucznik, C.A.; Egger, M.J.; Stanford, J.B. Characteristics of menstrual cycles with or without intercourse in women with no known subfertility. Hum. Reprod. Open 2022, 2022, hoac039. [Google Scholar] [CrossRef] [PubMed]
- Park, Y.J.; Shin, H.; Jeon, S.; Cho, I.; Kim, Y.J. Menstrual Cycle Patterns and the Prevalence of Premenstrual Syndrome and Polycystic Ovary Syndrome in Korean Young Adult Women. Healthcare 2021, 9, 56. [Google Scholar] [CrossRef]
- Zurawiecka, M.; Wronka, I. The Influence of Age at Menarche on the Menstrual Pattern of Polish University Students. J. Adolesc. Health 2021, 68, 210–212. [Google Scholar] [CrossRef]
- Mao, L.; Xi, S.; Bai, W.; Yao, C.; Zhou, Y.; Chen, X.; Sun, Y. Menstrual patterns and disorders among Chinese women of reproductive age: A cross-sectional study based on mobile application data. Medicine 2021, 100, e25329. [Google Scholar] [CrossRef] [PubMed]
- Belsey, E.M.; d’Arcangues, C.; Carlson, N. Determinants of menstrual bleeding patterns among women using natural and hormonal methods of contraception. II. The influence of individual characteristics. Contraception 1988, 38, 243–257. [Google Scholar] [CrossRef] [PubMed]
- Santos, I.S.; Minten, G.C.; Valle, N.C.; Tuerlinckx, G.C.; Silva, A.B.; Pereira, G.A.; Carriconde, J.F. Menstrual bleeding patterns: A community-based cross-sectional study among women aged 18–45 years in Southern Brazil. BMC Womens Health 2011, 11, 26. [Google Scholar] [CrossRef]
- Kafaei-Atrian, M.; Mohebbi-Dehnavi, Z.; Sayadi, L.; Asghari-Jafarabadi, M.; Karimian-Taheri, Z.; Afshar, M. The relationship between the duration of menstrual bleeding and obesity-related anthropometric indices in students. J. Educ. Health Promot. 2019, 8, 81. [Google Scholar] [PubMed]
- Parker, M.A.; Sneddon, A.E.; Arbon, P. The menstrual disorder of teenagers (MDOT) study: Determining typical menstrual patterns and menstrual disturbance in a large population-based study of Australian teenagers. BJOG 2010, 117, 185–192. [Google Scholar] [CrossRef]
- Belsey, E.M.; Peregoudov, S.; Task Force on Long-Acting Systemic Agents for Fertility Regulation. Determinants of menstrual bleeding patterns among women using natural and hormonal methods of contraception I. Regional variation. Contraception 1988, 38, 227–242. [Google Scholar] [CrossRef]
- Snowden, R.; Christian, B. Patterns and Perceptions of Menstruation: A World Health Organisation International Study; Croom Helm, London and Canberra and St. Martin’s Press: New York, NY, USA, 1983. [Google Scholar]
- Hallberg, L.; Högdahl, A.M.; Nilsson, L.; Rybo, G. Menstrual blood loss--a population study. Variation at different ages and attempts to define normality. Acta Obs. Gynecol. Scand. 1966, 45, 320–351. [Google Scholar] [CrossRef]
- Ji, G.; Ma, L.Y.; Zeng, S.; Fan, H.M.; Han, L.H. Menstrual blood loss in healthy Chinese women. Contraception 1981, 23, 591–601. [Google Scholar] [CrossRef]
- Matsumoto, S.; Tamada, T.; Konuma, S. Endocrinological analysis of environmental menstrual disorders. Int. J. Fertil. 1979, 24, 233–239. [Google Scholar]
- Collett, M.E.; Wertenberger, G.E.; Fiske, V.M. The effect of age upon the pattern of the menstrua cycle. Fertil. Steril. 1954, 45, 437–448. [Google Scholar] [CrossRef]
- Prill, H.J.; Maar, H. Zyklusveränderungen bei Höhenaufenthalt [Cycle changes when staying in high altitude]. Med. Klin. 1971, 66, 986–989. [Google Scholar]
- Bayer, S.R.; DeCherney, A.H. Clinical manifestations and treatment of dysfunctional uterine bleeding. JAMA 1993, 269, 1823–1828. [Google Scholar] [CrossRef]
- Van Voorhis, B.J.; Santoro, N.; Harlow, S.; Crawford, S.L.; Randolph, J. The relationship of bleeding patterns to daily reproductive hormones in women approaching menopause. Obs. Gynecol. 2008, 112, 101–108. [Google Scholar] [CrossRef]
- Treloar, A. Menstrual Cyclicity and the Pre-Menopause. Maturitas 1981, 3, 249–264. [Google Scholar] [CrossRef]
- Lenton, E.A.; Landgren, B.M.; Sexton, L.; Harper, R. Normal variation in the length of the follicular phase of the menstrual cycle. Br. J. Obs. Gynecol. 1984, 91, 681–684. [Google Scholar] [CrossRef] [PubMed]
- Lenton, E.A.; Landgren, B.M.; Sexton, L. Normal variation in the length of the luteal phase of the menstrual cycle. Br. J. Obs. Gynecol. 1984, 91, 685–689. [Google Scholar] [CrossRef]
- Lenton, E.A.; Lawrence, G.F.; Coleman, R.A.; Cooke, I.D. Individual variation in gonadotrophin and steroid concentrations and in the lengths of the follicular and luteal phases in women with regular menstrual cycles. Clin. Reprod. Fertil. 1983, 2, 143–150. [Google Scholar]
- Cole, L.A.; Ladner, D.G.; Byrn, F.W. The normal variabilities of the menstrual cycle. Fertil. Steril. 2009, 91, 522–527. [Google Scholar] [CrossRef] [PubMed]
- Harlow, S.D.; Campbell, B.C. Host factors that influence the duration of menstrual bleeding. Epidemiology 1994, 5, 352–355. [Google Scholar] [CrossRef] [PubMed]
- Benn, R.T. Some mathematical properties of weight-for-height indices used as measures of adiposity. Br. J. Prev. Soc. Med. 1971, 25, 42–50. [Google Scholar] [CrossRef]
- Harlow, S.D.; Campbell, B. Ethnic differences in the duration and amount of menstrual bleeding during the postmenarcheal period. Am. J. Epidemiol. 1996, 144, 980–988. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization Task Force on Adolescent Reproductive Health. World Health Organization multicenter study on menstrual and ovulatory patterns in adolescent girls. II. Longitudinal study of menstrual patterns in the early postmenarcheal period, duration of bleeding episodes and menstrual cycles. J. Adolesc. Health Care 1986, 7, 236–244. [Google Scholar] [CrossRef]
- Harlow, S.D.; Ephross, S.A. Epidemiology of menstruation and its relevance to women’s health. Epidemiol. Rev. 1995, 17, 265–286. [Google Scholar] [CrossRef] [PubMed]
- Nikolova, P.P.; Negrev, N.N.; Nikolova, R.I.; Dzhebarov, S.S. Menstrual Rhythm, Menstrual Interval, and Duration of Menstruation in Left-Handed and Right-Handed Women. Hum. Physiol. 2003, 29, 390–391. [Google Scholar] [CrossRef]
- Tan, U. Testosterone and estradiol in right-handed men but only estradiol in right-handed women is inversely correlated with the degree of right-hand preference. Int. J. Neurosci. 1992, 66, 25–34. [Google Scholar] [CrossRef]
- Kennedy, K.E.R.; Onyeonwu, C.; Nowakowski, S.; Hale, L.; Branas, C.C.; Killgore, W.D.S.; Wills, C.C.A.; Grandner, M.A. Menstrual regularity and bleeding is associated with sleep duration, sleep quality and fatigue in a community sample. J. Sleep Res. 2022, 31, e13434. [Google Scholar] [CrossRef]
- Mollabashi, E.N.; Ziaie, T.; Bekhradi, R.; Khalesi, Z.B. Do Chamomile effect on duration, amount of bleeding, and interval of menstrual cycles? J. Pharmacopunct. 2020, 23, 25–29. [Google Scholar] [CrossRef]
- Chang, P.J.; Chen, P.C.; Hsieh, C.J.; Chiu, L.T. Risk factors on the menstrual cycle of healthy Taiwanese college nursing students. Aust. N. Z. J. Obs. Gynecol. 2009, 49, 689–694. [Google Scholar] [CrossRef]
- Tayebi, N.; Yazdanpanahi, Z.; Yektatalab, S.; Pourahmad, S.; Akbarzadeh, M. The Relationship Between Body Mass Index (BMI) and Menstrual Disorders at Different Ages of Menarche and Sex Hormones. J. Natl. Med. Assoc. 2018, 110, 440–447. [Google Scholar] [CrossRef]
- Zhang, Y.; Ji, L.; Hu, Y.; Tse, L.A.; Wang, Y.; Qin, K.; Ding, G.; Zhou, Y.; Yu, X.; Shanghai Birth Cohort Study; et al. Exposure to Organophosphate Pesticides and Menstrual Cycle Characteristics in Chinese Preconceptional Women. Am. J. Epidemiol. 2020, 189, 375–383. [Google Scholar] [CrossRef]
- Wood, C.; Larsen, L.; Williams, R. Menstrual characteristics of 2,343 women attending the Shepherd Foundation. Aust. N. Z. J. Obs. Gynecol. 1979, 19, 107–110. [Google Scholar] [CrossRef]
- Kirchengast, S. Intercorrelations between menstrual cycle patterns and body dimensions in Austrian women. J. Biosoc. Sci. 1994, 26, 207–216. [Google Scholar] [CrossRef] [PubMed]
- Fakeye, O.; Adegoke, A. The characteristics of the menstrual cycle in Nigerian schoolgirls and the implications for school health programmes. Afr. J. Med. Med. Sci. 1994, 23, 13–17. [Google Scholar] [PubMed]
- Vercellini, P.; De Giorgi, O.; Aimi, G.; Panazza, S.; Uglietti, A.; Crosignani, P.G. Menstrual characteristics in women with and without endometriosis. Obs. Gynecol. 1997, 90, 264–268. [Google Scholar] [CrossRef]
- Bata, M.S. Age at menarche, menstrual patterns, and menstrual characteristics in Jordanian adolescent girls. Int. J. Gynecol. Obs. 2012, 119, 281–283. [Google Scholar] [CrossRef]
- Rigon, F.; De Sanctis, V.; Bernasconi, S.; Bianchin, L.; Bona, G.; Bozzola, M.; Buzi, F.; Radetti, G.; Tatò, L.; Tonini, G.; et al. Menstrual pattern and menstrual disorders among adolescents: An update of the Italian data. Ital. J. Pediatr. 2012, 38, 38. [Google Scholar] [CrossRef] [PubMed]
- Farahmand, S.K.; Emadzadeh, M.; Hassankhani, G.G.; Mirbirjandian, M.; Rafiezadeh, T.; Abasalti, Z.; Khayyatzadeh, S.S.; Bahrami, A.; Tabatabaeizadeh, S.A.; Tayefi, M.; et al. The relationship between short stature and menstrual pattern in a large cohort of Iranian girls. J. Obs. Gynecol. 2020, 40, 228–232. [Google Scholar] [CrossRef]
- Ansong, E.; Arhin, S.K.; Cai, Y.; Xu, X.; Wu, X. Menstrual characteristics, disorders and associated risk factors among female international students in Zhejiang Province, China: A cross-sectional survey. BMC Womens Health 2019, 19, 35. [Google Scholar] [CrossRef]
- Charis, A.C.; Rawat, N.; Zachariah, K. Menstrual changes after spinal cord injury. Spinal Cord 2022, 60, 712–715. [Google Scholar] [CrossRef]
- Maybin, J.A.; Critchley, H.O. Menstrual physiology: Implications for endometrial pathology and beyond. Hum. Reprod. Update 2015, 21, 748–761. [Google Scholar] [CrossRef]
- Critchley, H.O.D.; Maybin, J.A.; Armstrong, G.M.; Williams, A.R.W. Physiology of the Endometrium and Regulation of Menstruation. Physiol. Rev. 2020, 100, 1149–1179. [Google Scholar] [CrossRef]
- Brenner, R.M.; Nayak, N.R.; Slayden, O.D.; Critchley, H.O.; Kelly, R.W. Premenstrual and menstrual changes in the macaque and human endometrium: Relevance to endometriosis. Ann. N. Y. Acad. Sci. 2002, 955, 60–406. [Google Scholar] [CrossRef]
- Catalano, R.D.; Critchley, H.O.; Heikinheimo, O.; Baird, D.T.; Hapangama, D.; Sherwin, J.R.A.; Charnock-Jones, D.S.; Smith, S.K.; Sharkey, A.M. Mifepristone induced progesterone withdrawal reveals novel regulatory pathways in human endometrium. Mol. Hum. Reprod. 2007, 13, 641–654. [Google Scholar] [CrossRef] [PubMed]
- Evans, J.; Salamonsen, L.A. Decidualized human endometrial stromal cells are sensors of hormone withdrawal in the menstrual inflammatory cascade. Biol. Reprod. 2014, 90, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Henriet, P.; Gaide Chevronnay, H.P.; Marbaix, E. The endocrine and paracrine control of menstruation. Mol. Cell. Endocrinol. 2012, 358, 197–207. [Google Scholar] [CrossRef]
- Salamonsen, L.A.; Woolley, D.E. Menstruation: Induction by matrix metalloproteinases and inflammatory cells. J. Reprod. Immunol. 1999, 44, 1–27. [Google Scholar] [CrossRef]
- Hisamatsu, Y.; Murata, H.; Tsubokura, H.; Hashimoto, Y.; Kitada, M.; Tanaka, S.; Okada, H. Matrix Metalloproteinases in Human Decidualized Endometrial Stromal Cells. Curr. Issues Mol. Biol. 2021, 43, 2111–2123. [Google Scholar] [CrossRef] [PubMed]
- Reavey, J.J.; Walker, C.; Nicol, M.; Murray, A.A.; Critchley, H.O.D.; Kershaw, L.E.; Maybin, J.A. Markers of human endometrial hypoxia can be detected in vivo and ex vivo during physiological menstruation. Hum. Reprod. 2021, 36, 941–950. [Google Scholar] [CrossRef]
- Schröder, R. Anatomische studien zur normalen und patholgishen physiologie des menstrual zyklus. Arch. Gynäkol. 1915, 104, 27–103. [Google Scholar] [CrossRef]
- Bartelmez, G.W. The phases of the menstrual cycle and their interpretation in terms of pregnancy cycle. Am. J. Obs. Gynecol. 1957, 74, 931–955. [Google Scholar] [CrossRef]
- Maughs, G.M.B. Menstruation, or the Menstrual Flow, an Epiphenomenon of Ovulation. An Argumental Treatise, Read before the St. Louis Medical Society, on the Question: Is Menstruation Ovulation? PM Pinckard: St Louis, MO, USA,, 1867. [Google Scholar]
- Hitschmann, F.; Adler, L. Der bau der uterusschleimhaut des geschlechtsreifen weibes mit besonderer berücksichtigung der menstruation. Monatsschrift Für Geburtshilfe Und Gynäkologie 1908, 27, 1–82. [Google Scholar]
- Markee, J.E. Menstruation in intraocular endometrial transplants in the rhesus monkey. Contrib. Embryol. 1940, 177, 221–308. [Google Scholar]
- Markee, J.E. Morphological basis for menstrual bleeding. Relation of regression to the initiation of bleeding. Bull. N. Y. Acad. Med. 1948, 24, 253–268. [Google Scholar] [PubMed]
- Bartelmez, G.W. Glandular physiology and therapy. Menstruation. JAMA 1941, 116, 702–704. [Google Scholar] [CrossRef]
- Sixma, J.J.; Christiaens, G.C.; Haspels, A.A. The sequence of haemostatic events in the endometrium during normal menstruation. In Endometrial Bleeding and Steroidal Contraception, Proceedings of a Symposium on Steroid Contraception and Mechanisms of endometrial Bleeding, Geneva, Switzerland, 12–14 September 1979; Diczfalusy, E., Fraser, I.S., Webb, F.T., Eds.; Pitman Press Ltd.: Bath, UK, 1980; pp. 86–96. [Google Scholar]
- Cristiaens, G.C.; Sixma, J.J.; Haspels, A.A. Morphological aspects of menstrual bleeding: Possible influences of IUD. In Proceedings of the International Symposium on Medicated IUD’s and Polymetric Delivery Systems, Amsterdam, The Netherlands, 27–30 June 1979; p. 43. [Google Scholar]
- Rock, J.; Bartlett, M.K. Biopsy studies of human endometrium: Criteria of dating and information about amenorrhea, menorrhagia, and time of ovulation. J. Am. Med. Assoc. 1937, 108, 2022–2028. [Google Scholar] [CrossRef]
- Nogales-Ortiz, F.; Puerta, J.; Nogales, F.F., Jr. The normal menstrual cycle. Chronology and mechanism of endometrial desquamation. Obs. Gynecol. 1978, 51, 259–264. [Google Scholar] [CrossRef]
- Flowers, C.E., Jr.; Wilborn, W.H. New observations on the physiology of menstruation. Obs. Gynecol. 1978, 51, 16–24. [Google Scholar]
- Weber, M. Die hormonale Therapie der durch “verzögerte Abstoßung“ bedingten Blutungsstörung. [Hormone therapy of menstrual disorders due to delayed discharge]. Geburtshilfe Frauenheilkd 1954, 14, 710. [Google Scholar]
- Sturdee, D.W.; Barlow, D.H.; Ulrich, L.G.; Wells, M.; Gydesen, H.; Campbell, M.; O’Brien, K.; Vessey, M. Is the timing of withdrawal bleeding a guide to endometrial safety during sequential oestrogen-progestagen replacement therapy? UK Continuous Combined HRT Study Investigators. Lancet 1994, 344, 979–982. [Google Scholar] [CrossRef]
- Devoto, L.; Vega, M.; Navarro, V.; Sir, T.; Alba, F.; Castro, O. Regulation of steroid hormone synthesis by human corpora lutea: Failure of follicle stimulating hormone to support steroidogenesis in vivo and in vitro. Fertil. Steril. 1989, 51, 628–633. [Google Scholar] [CrossRef]
- Devoto, L.; Fuentes, A.; Kohen, P.; Céspedes, P.; Palomino, A.; Pommer, R.; Muñoz, A.; Strauss, J.F., 3rd. The human corpus luteum: Life cycle and function in natural cycles. Fertil. Steril. 2009, 92, 1067–1079. [Google Scholar] [CrossRef]
- Stocco, C.; Telleria, C.; Gibori, G. The Molecular Control of Corpus Luteum Formation, Function, and Regression. Endocr. Rev. 2007, 28, 117–149. [Google Scholar] [CrossRef] [PubMed]
- Baerwald, A.R.; Adams, G.P.; Pierson, R.A. Characterization of ovarian follicular wave dynamics in women. Biol. Reprod. 2003, 69, 1023–1031. [Google Scholar] [CrossRef]
- Block, E. Quantitative morphological investigations of the follicular system in women: Variations in the different phases of the sexual cycle. Acta Endocrinol. 1951, 8, 33–54. [Google Scholar]
- Gougeon, A. Dynamics of follicular growth in the human: A model from preliminary results. Hum. Reprod. 1986, 1, 81–87. [Google Scholar] [CrossRef]
- Vanden Brink, H.; Robertson, D.M.; Lim, H.; Lee, C.; Chizen, D.; Harris, G.; Hale, G.; Burger, H.; Baerwald, A. Associations between antral ovarian follicle dynamics and hormone production throughout the menstrual cycle as women age. J. Clin. Endocrinol. Metab. 2015, 100, 4553–4562. [Google Scholar] [CrossRef]
- Santoro, N.; Rosenberg Brown, J.; Adel, T.; Skurnick, J.H. Characterization of Reproductive Hormonal Dynamics in the Perimenopause. J. Clin. Endocrinol. Metab. 1996, 81, 1495–1501. [Google Scholar] [PubMed]
- Hale, G.E.; Hughes, C.L.; Burger, H.G.; Robertson, D.M.; Fraser, I.S. Atypical estradiol secretion and ovulation patterns caused by luteal out of phase (LOOP) events underlying irregular ovulatory menstrual cycles in the menopausal transition. Menopause 2009, 16, 50–59. [Google Scholar] [CrossRef]
- Baerwald, A.; Vanden Brink, H.; Hunter, C.; Beuker, D.; Lim, H.; Lee, C.H.; Chizen, D. Age-related changes in luteal dynamics: Preliminary associations with antral follicular dynamics and hormone production during the human menstrual cycle. Menopause 2018, 25, 399–407. [Google Scholar] [CrossRef]
- Baerwald, A.; Pierson, R. Ovarian follicular waves during the menstrual cycle: Physiologic insights into novel approaches for ovarian stimulation. Fertil. Steril. 2020, 114, 443–457. [Google Scholar] [CrossRef]
- Devoto, L.; Kohen, P.; Muñoz, A.; Strauss, J.F. 3rd. Human corpus luteum physiology and the luteal-phase dysfunction associated with ovarian stimulation. Reprod. Biomed. Online 2009, 18 (Suppl. 2), 19–24. [Google Scholar] [CrossRef] [PubMed]
- Pattnaik, S.; Das, D.; Venkatesan, V.A.; Rai, A. Predicting serum hormone concentration by estimation of urinary hormones through a home-use device. Hum. Reprod. Open 2022, 2023, hoac058. [Google Scholar] [CrossRef]
- Crawford, N.M.; Pritchard, D.A.; Herring, A.H.; Steiner, A.Z. Prospective evaluation of luteal phase length and natural fertility. Fertil. Steril. 2017, 107, 749–755. [Google Scholar] [CrossRef]
- Schliep, K.C.; Mumford, S.L.; Hammoud, A.O.; Stanford, J.B.; Kissell, K.A.; Sjaarda, L.A.; Perkins, N.J.; Ahrens, K.A.; Wactawski-Wende, J.; Mendola, P.; et al. Luteal phase deficiency in regularly menstruating women: Prevalence and overlap in identification based on clinical and biochemical diagnostic criteria. J. Clin. Endocrinol. Metab. 2014, 99, E1007–E1014. [Google Scholar] [CrossRef] [PubMed]
- Duncan, W.C.; McNeilly, A.S.; Fraser, H.M.; Illingworth, P.J. Luteinizing hormone receptor in the human corpus luteum: Lack of down-regulation during maternal recognition of pregnancy. Hum. Reprod. 1996, 11, 2291–2297. [Google Scholar] [CrossRef] [PubMed]
- Zeleznik, A.J. In vivo responses of the primate corpus luteum to luteinizing hormone and chorionic gonadotropin. Proc. Natl. Acad. Sci. USA 1998, 95, 11002–11007. [Google Scholar] [CrossRef]
- Devoto, L.; Vega, M.; Kohen, P.; Castro, O.; Carvallo, P.; Palomino, A. Molecular regulation of progesterone secretion by the human corpus luteum throughout the menstrual cycle. J. Reprod. Immunol. 2002, 55, 11–20. [Google Scholar] [CrossRef]
- Fraser, H.M.; Lunn, S.F.; Harrison, D.J.; Kerr, J.B. Luteal regression in the primate: Different forms of cell death during natural and gonadotropin-releasing hormone antagonist or prostaglandin analogue-induced luteolysis. Biol. Reprod. 1999, 61, 1468–1479. [Google Scholar] [CrossRef]
- Devoto, L.; Henríquez, S.; Kohen, P.; Strauss, J.F., 3rd. The significance of estradiol metabolites in human corpus luteum physiology. Steroids 2017, 123, 50–54. [Google Scholar] [CrossRef]
- Hirama, Y.; Ochiai, K. Estrogen and progesterone receptors of the out-of-phase endometrium in female infertile patients. Fertil. Steril. 1995, 63, 984–988. [Google Scholar] [CrossRef]
- Jones, G. The luteal phase defect. Fertil. Steril. 1976, 27, 351–356. [Google Scholar] [CrossRef]
- Fritz, M.A. Inadequate luteal function and recurrent abortion: Diagnosis and treatment of luteal phase deficiency. Semin. Reprod. Med. 1988, 6, 129–144. [Google Scholar] [CrossRef]
- Coutifaris, C.; Myers, E.R.; Guzick, D.S.; Diamond, M.P.; Carson, S.A.; Legro, R.S.; McGovern, P.G.; Schlaff, W.D.; Carr, B.R.; NICHD National Cooperative Reproductive Medicine Network; et al. Histological dating of timed endometrial biopsy tissue is not related to fertility status. Fertil. Steril. 2004, 82, 1264–1272. [Google Scholar] [CrossRef] [PubMed]
- Murray, M.J.; Meyer, W.R.; Zaino, R.J.; Lessey, B.A.; Novotny, D.B.; Ireland, K.; Zeng, D.; Fritz, M.A. A critical analysis of the accuracy, reproducibility, and clinical utility of histologic endometrial dating in fertile women. Fertil. Steril. 2004, 81, 1333–1343. [Google Scholar] [CrossRef] [PubMed]
- Scott, R.T.; Snyder, R.R.; Bagnall, J.W.; Reed, K.D.; Adair, C.F.; Hensley, S.D. Evaluation of the impact of intraobserver variability on endometrial dating and the diagnosis of luteal phase defects. Fertil. Steril. 1993, 60, 652–657. [Google Scholar] [CrossRef]
- Driessen, F.; Holwerda, P.J.; vd Putte, S.C.; Kremer, J. The significance of dating an endometrial biopsy for the prognosis of the infertile couple. Int. J. Fertil. 1980, 25, 112–116. [Google Scholar]
- Santoro, N.; Goldsmith, L.T.; Heller, D.; Illsley, N.; McGovern, P.; Molina, C.; Peters, S.; Skurnick, J.H.; Forst, C.; Weiss, G. Luteal progesterone relates to histological endometrial maturation in fertile women. J. Clin. Endocrinol. Metab. 2000, 85, 4207–4211. [Google Scholar] [CrossRef]
- Bassil, R.; Casper, R.; Samara, N.; Hsieh, T.B.; Barzilay, E.; Orvieto, R.; Haas, J. Does the endometrial receptivity array really provide personalized embryo transfer? J. Assist. Reprod. Genet. 2018, 35, 1301–1305. [Google Scholar] [CrossRef] [PubMed]
- Churchill, S.; Comstock, I.; Lathi, R. Pregnancy outcomes after endometrial receptivity array in an infertile population. Fertil. Steril. 2017, 108, e360. [Google Scholar] [CrossRef]
- Riestenberg, C.; Kroener, L.; Quinn, M.; Ching, K.; Ambartsumyan, G. Routine endometrial receptivity array in first embryo transfer cycles does not improve live birth rate. Fertil. Steril. 2021, 115, 1001–1006. [Google Scholar] [CrossRef]
- Alfer, J.; Fattahi, A.; Bleisinger, N.; Krieg, J.; Behrens, R.; Dittrich, R.; Beckmann, M.W.; Hartmann, A.; Classen-Linke, I.; Popovici, R.M. Endometrial Dating Method Detects Individual Maturation Sequences During the Secretory Phase [published correction appears in In Vivo. 2020, 34, 3055]. Vivo 2020, 34, 1951–1963. [Google Scholar] [CrossRef]
- Usadi, R.S.; Groll, J.M.; Lessey, B.A.; Lininger, R.A.; Zaino, R.J.; Fritz, M.A.; Young, S.L. Endometrial development and function in experimentally induced luteal phase deficiency. J. Clin. Endocrinol. Metab. 2008, 93, 4058–4064. [Google Scholar] [CrossRef]
- Samavat, H.; Kurzer, M.S. Estrogen metabolism and breast cancer. Cancer Lett. 2015, 356 Pt A, 231–243. [Google Scholar] [CrossRef]
- Comstock, I.A.; Diaz-Gimeno, P.; Cabanillas, S.; Bellver, J.; Sebastian-Leon, P.; Shah, M.; Schutt, A.; Valdes, C.T.; Ruiz-Alonso, M.; Valbuena, D.; et al. Does an increased body mass index affect endometrial gene expression patterns in infertile patients? A functional genomics analysis. Fertil. Steril. 2017, 107, 740–748. [Google Scholar] [CrossRef] [PubMed]
- Noyes, R.W.; Hertig, A.T.; Rock, J. Dating the endometrial biopsy. Fertil. Steril. 1950, 1, 3–25. [Google Scholar] [CrossRef]
- Maybin, J.; Critchley, H. Repair and regeneration of the human endometrium. Expert. Rev. Obs. Gynecol. 2009, 4, 283–298. [Google Scholar] [CrossRef]
- Salamonsen, L.A. Tissue injury and repair in the female human reproductive tract. Reproduction 2003, 125, 301–311. [Google Scholar] [CrossRef] [PubMed]
- Padykula, H.A.; Coles, L.G.; Okulicz, W.C.; Rapaport, S.I.; McCracken, J.A.; King, N.W., Jr.; Longcope, C.; Kaiserman-Abramof, I.R. The basalis of the primate endometrium: A bifunctional germinal compartment. Biol. Reprod. 1989, 40, 681–690. [Google Scholar] [CrossRef]
- Bohnen, P. Wie weit wird das Endometrium bei der Menstruation abgestoßen? [How deeply is the endometrium shed during menstruation?]. Arch. Gynäkol. 1927, 129, 459–472. [Google Scholar] [CrossRef]
- Ferenczy, A. Studies on the cytodynamics of human endometrial regeneration. I. Scanning electron microscopy. Am. J. Obs. Gynecol. 1976, 124, 64–74. [Google Scholar] [CrossRef]
- Baggish, M.S.; Pauerstein, C.J.; Woodruff, J.D. Role of stroma in regeneration of endometrial epithelium. Am. J. Obs. Gynecol. 1967, 99, 459–465. [Google Scholar] [CrossRef]
- Nogales-Ortiz, F.; Nogales, F.F. Endometrial regeneration under physiological and pathological conditions. In Endometrial Bleeding and Steroidal Contraception, Proceedings of the Symposium on Steroid Contraception and Mechanisms of Endometrial Bleeding, WHO, Geneva, Switzerland, 12–14 September 1979; Diczfalusy, E., Fraser, I.S., Webb, E.T.G., Eds.; Pitman Press Ltd.: Bath, UK, 1980. [Google Scholar]
- Ferenczy, A. Studies on the cytodynamics of human endometrial regeneration. II. Transmission electron microscopy and histochemistry. Am. J. Obs. Gynecol. 1976, 124, 582–595. [Google Scholar] [CrossRef]
- Ferenczy, A.; Bergeron, C. Histology of the human endometrium: From birth to senescence. Ann N Y Acad Sci 1991, 622, 6–27. [Google Scholar] [CrossRef] [PubMed]
- Dallenbach, F.D.; Dallenbach-Hellweg, G. Immunohistologische Untersuchungen zur Lokalisation des Relaxins in menschlicher Plazenta und Dezidua [Immunohistological studies on the localization of relaxin in human placenta and decidua]. Virchows Arch. [Pathol. Anat.] 1964, 337, 301. [Google Scholar] [CrossRef]
- Garry, R.; Hart, R.; Karthigasu, K.A.; Burke, C. A re-appraisal of the morphological changes within the endometrium during menstruation: A hysteroscopic, histological and scanning electron microscopic study. Hum. Reprod. 2009, 24, 1393–1401. [Google Scholar] [CrossRef]
- Gargett, C.E.; Chan, R.W.; Shwab, K.E. Endometrial stem cells. Curr. Opin. Obs. Gynecol. 2007, 19, 377–383. [Google Scholar] [CrossRef] [PubMed]
- Lynch, L.; Golden-Mason, L.; Eogan, M.; O’Herlihy, C.; O’Farrally, C. Cells with haematopoeitic stem cell phenotype in adult endometrium: Relevance to infertility. Hum. Reprod. 2007, 22, 919–926. [Google Scholar] [CrossRef]
- Bratincsak, A.; Brownstein, M.J.; Cassiani-Ingoni, R.; Pastorino, S.; Szalayova, I.; Toth, Z.E.; Key, S.; Nemeth, K.; Pickel, J.; Mezey, E. CD45-positive blood cells give rise to uterine epithelial cells in mice. Stem Cells 2007, 25, 2820–2826. [Google Scholar] [CrossRef]
- Roth, L.P.; Haley, K.M.; Baldwin, M.K. A retrospective comparison of time to cessation of acute heavy menstrual bleeding in adolescents following two dose regimens of combined oral hormonal therapy. J. Pediatr. Adolesc. Gynecol. 2022, 35, 294–298. [Google Scholar] [CrossRef]
Study | Suggested Cut-Off for Normal |
---|---|
Meigs (1849) [13] | Each woman has her own cycle |
Tauszky (1879) [14] | 10 days can be considered normal |
Fraser et al (2007) [7] | Between 4.5–8 days |
Munro et al (2018) [9] | upper limit of normal > 8 days as, no lower limit |
Bastianelli et al (2023) [10] | Women reported preference of 3 days |
BMI Range | Number of Cycles | Duration of Bleeding (Mean ± Std) |
---|---|---|
15–18.5 | 25,735 | 4.2 ± 1.5 * |
18.5–25 | 431,667 | 4.0 ± 1.5 |
25–30 | 100,228 | 3.9 ± 1.4 * |
30–35 | 26,483 | 3.9 ± 1.4 * |
35–50 | 12,011 | 3.0 ± 1.5 * |
All cycles | 621,613 | 4.0 ± 1.5 |
Study | Observation Related to Duration of Bleeding |
---|---|
Bastianelli et al (2023) [10] | Women regard 3 days as the optimal duration of bleeding |
Zhang et al (2017) [12] | Women who reported their bleeding to last <4 or >5 days had lower fecundity ratio compared to those who reported 4–5 days of bleeding |
Najmabadi et al (2020) [28] | No difference in duration of bleeding based on age (<30 years vs ≥30 years) or parity (nulliparous vs parous) |
Belsey and Pinol (1997) [29] | Mean duration reduced from 6.6 days at 15 y, to 6.0 days by 20 y and remained largely unchanged until age 49 y |
Dasharathy et al (2012) [41] | Longer duration of bleeding in ovulatory compared to anovulatory cycles |
Zurawiecka et al (2021) [44] | No difference in the duration of bleeding between women with early, average, or late menarche |
Mao et al (2021) [45] | Prolonged bleeding in underweight and shorter bleeding in obese women |
Kafaei-Atrian et al (2019) [48] | Duration of bleeding had a significant relationship with weight, and the circumference of waist, hip and arm. A significant relationship between duration and waist-to-height, waist-to-hip, hip-to-height and arm-to-height ratios |
Van Voorhis et al (2008) [58] | Self-reported past diagnosis of fibroids linked to longer duration of bleeding |
Harlow and Campbell (1994) [64] | The duration of bleeding not associated with the length of the preceding cycles, history of long cycles, change in body weight, college entry, or being away from home. Slight increase if late menarche. Longer bleeding if low weight-for-height. |
WHO Task Force (1986) [67] | The duration of bleeding varied between countries and is slightly longer if late menarche. Unaffected by exercise, previous cycle length or gynecologic age. |
Nikolova et al (2003) [69] | The duration of bleeding (4.69 ± 0.05 days) was significantly shorter in left-handed compared to right-handed women (5.75 ± 0.004 days) |
Mollabashi et al (2020) [72] | Duration of bleeding not affected by Chamomile |
Chang et al (2009) [73] | Duration of bleeding linked to obesity |
Tayebi et al (2018) [74] | Link between duration of bleeding and obesity not confirmed |
Zhang et al (2020) [75] | Exposure to high concentration of organophosphate pesticides linked to shorter duration of bleeding |
Wood et al (1979) [76] | Based on patient recollection, the duration of bleeding was 1–7 days and 3% of women bled for >7 days |
Kirchengast (1994) [77] | The post-cephalic height and length dimensions were positively correlated with the duration of bleeding |
Fakeye and Adegoke (1994) [78] | Prolonged bleeding (≥8 days) occurred in less than 5% of postmenarcheal schoolgirls |
Vercellini et al (1997) [79] | The duration of bleeding was longer (mean difference 0.33 days) in women with endometriosis |
Bata (2012) [80] | The duration of bleeding in 73.6% of secondary school students was between 4–7 days. |
Rigon et al (2012) [81] | In women and girls aged (13–21 years), the average duration of bleeding was <4 days in 3.2% of participants and >6 days in 19% of participants |
Farahmand et al (2020) [82] | No difference in the duration of bleeding in postmenarcheal girls with different height centiles |
Ansong et al (2020) [83] | International students in China who had high levels of stress reported abnormal duration of bleeding |
Charis et al (2022) [84] | In women recovering from spinal cord injury, the mean duration of bleeding was lower (4.28 ± 0.96 days) compared to the duration of bleeding before the injury (4.88 ± 0.4 days) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Habiba, M.; Benagiano, G. The Duration of Menstrual Blood Loss: Historical to Current Understanding. Reprod. Med. 2023, 4, 145-165. https://doi.org/10.3390/reprodmed4030015
Habiba M, Benagiano G. The Duration of Menstrual Blood Loss: Historical to Current Understanding. Reproductive Medicine. 2023; 4(3):145-165. https://doi.org/10.3390/reprodmed4030015
Chicago/Turabian StyleHabiba, Marwan, and Giuseppe Benagiano. 2023. "The Duration of Menstrual Blood Loss: Historical to Current Understanding" Reproductive Medicine 4, no. 3: 145-165. https://doi.org/10.3390/reprodmed4030015
APA StyleHabiba, M., & Benagiano, G. (2023). The Duration of Menstrual Blood Loss: Historical to Current Understanding. Reproductive Medicine, 4(3), 145-165. https://doi.org/10.3390/reprodmed4030015