Skip to main content

Advertisement

SpringerLink
Log in

The risk of endometriosis by early menarche is recently increased: a meta-analysis of literature published from 2000 to 2020

  • Review
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Purpose

The relationship between menarche age and endometriosis has been studied extensively; however, the results were inconsistent due to differences in study dates, populations, and methodology. The goal of this meta-analysis was to see how different research populations, dates, and types affected the estimated risk of endometriosis in early menarche.

Methods

The terms “endometriosis”, “early menarche”, and other pertinent terms were searched in PubMed, Medline, and Embase. This meta-analysis comprised 16 papers published between 2000 and 2020, with a start year ranging from 1989 to 2017. Random effects were used to examine endometriosis risks in these articles. Study start years, countries, types (case–control and cohort studies), and quality (Newcastle–Ottawa scale, NOS) were all taken into account in further stratified analysis and meta-regression analyses.

Results

Early menarche (< 12 years) was associated with a significant pooled risk of endometriosis with high heterogeneity (OR = 1.34, 95% CI 1.16–1.54, I2 = 72.0%). Stratified analysis showed that this risk was increased in studies started after 2000 (OR = 1.62, 95% CI 0.96–1.35, I2 = 74.4%), compared to those before 2000 (OR = 1.13, 95% CI 1.16–1.54, I2 = 40.7%); additionally, this risk was higher in low-income countries (OR = 2.11, 95% CI 1.55–2.87, I2 = 0%) than in other countries (OR = 1.25, 95% CI 1.09–1.43, I2 = 70.6%). These results were further confirmed by meta-regression analysis (both P values < 0.1). No significant differences were found between different study types and NOS scores.

Conclusion

Our results suggested an increasing risk of endometriosis with early menarche, which was more noticeable in low-income countries. Large-scale studies are warranted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Availability of data and materials

Not applicable.

Code availability

Not applicable.

References

  1. Armour M, Lawson K, Wood A, Smith CA, Abbott J (2019) The cost of illness and economic burden of endometriosis and chronic pelvic pain in Australia: a national online survey. PLoS ONE 14:e0223316. https://doi.org/10.1371/journal.pone.0223316

    Article  CAS  Google Scholar 

  2. Roomaney R, Kagee A (2018) Salient aspects of quality of life among women diagnosed with endometriosis: a qualitative study. J Health Psychol 23:905. https://doi.org/10.1177/1359105316643069

    Article  Google Scholar 

  3. Soliman AM, Surrey E, Bonafede M, Nelson JK, Castelli-Haley J (2018) Real-world evaluation of direct and indirect economic burden among endometriosis patients in the United States. Adv Ther 35:408. https://doi.org/10.1007/s12325-018-0667-3

    Article  Google Scholar 

  4. Lin YH, Chen YH, Chang HY, Au HK, Tzeng CR, Huang YH (2018) Chronic niche inflammation in endometriosis-associated infertility: current understanding and future therapeutic strategies. Int J Mol Sci. https://doi.org/10.3390/ijms19082385

    Article  Google Scholar 

  5. Practice Committee of the American Society for Reproductive M (2012) Endometriosis and infertility: a committee opinion. Fertil Steril 98:591. https://doi.org/10.1016/j.fertnstert.2012.05.031

    Article  Google Scholar 

  6. Farland LV, Missmer SA, Bijon A, Gusto G, Gelot A, Clavel-Chapelon F et al (2017) Associations among body size across the life course, adult height and endometriosis. Hum Reprod 32:1732. https://doi.org/10.1093/humrep/dex207

    Article  CAS  Google Scholar 

  7. Holoch KJ, Lessey BA (2010) Endometriosis and infertility. Clin Obstet Gynecol 53:429. https://doi.org/10.1097/GRF.0b013e3181db7d71

    Article  Google Scholar 

  8. Zullo F, Spagnolo E, Saccone G, Acunzo M, Xodo S, Ceccaroni M et al (2017) Endometriosis and obstetrics complications: a systematic review and meta-analysis. Fertil Steril 108:667. https://doi.org/10.1016/j.fertnstert.2017.07.019

    Article  Google Scholar 

  9. Nicolaus K, Brauer D, Sczesny R, Buhler K, Diebolder H, Runnebaum IB (2020) A two-third majority of infertile women exhibit endometriosis in pre-ART diagnostic hysteroscopy and laparoscopic chromopertubation: only one-third have a tubal obstruction. Arch Gynecol Obstet 301:1081. https://doi.org/10.1007/s00404-020-05479-5

    Article  CAS  Google Scholar 

  10. von Theobald P, Cottenet J, Iacobelli S, Quantin C (2016) Epidemiology of endometriosis in france: a large, nation-wide study based on hospital discharge data. Biomed Res Int 2016:3260952. https://doi.org/10.1155/2016/3260952

    Article  CAS  Google Scholar 

  11. Burney RO, Giudice LC (2012) Pathogenesis and pathophysiology of endometriosis. Fertil Steril 98:511. https://doi.org/10.1016/j.fertnstert.2012.06.029

    Article  CAS  Google Scholar 

  12. Lagana AS, Garzon S, Gotte M, Vigano P, Franchi M, Ghezzi F et al (2019) The pathogenesis of endometriosis: molecular and cell biology insights. Int J Mol Sci. https://doi.org/10.3390/ijms20225615

    Article  Google Scholar 

  13. Peterson CM, Johnstone EB, Hammoud AO, Stanford JB, Varner MW, Kennedy A et al (2013) Risk factors associated with endometriosis: importance of study population for characterizing disease in the ENDO Study. Am J Obstet Gynecol 208(451):e1. https://doi.org/10.1016/j.ajog.2013.02.040

    Article  Google Scholar 

  14. Parazzini F, Esposito G, Tozzi L, Noli S, Bianchi S (2017) Epidemiology of endometriosis and its comorbidities. Eur J Obstet Gynecol Reprod Biol 209:3. https://doi.org/10.1016/j.ejogrb.2016.04.021

    Article  CAS  Google Scholar 

  15. Wei M, Cheng Y, Bu H, Zhao Y, Zhao W (2016) Length of menstrual cycle and risk of endometriosis: a meta-analysis of 11 case-control studies. Medicine (Baltimore) 95:e2922. https://doi.org/10.1097/MD.0000000000002922

    Article  Google Scholar 

  16. Gaudineau A, Ehlinger V, Vayssiere C, Jouret B, Arnaud C, Godeau E (2010) Factors associated with early menarche: results from the French Health Behaviour in School-aged Children (HBSC) study. BMC Public Health 10:175. https://doi.org/10.1186/1471-2458-10-175

    Article  Google Scholar 

  17. Forman MR, Mangini LD, Thelus-Jean R, Hayward MD (2013) Life-course origins of the ages at menarche and menopause. Adolesc Health Med Ther 4:1. https://doi.org/10.2147/AHMT.S15946

    Article  Google Scholar 

  18. Emons G, Grundker C, Hanf V (2002) Are estrogens carcinogens? Zentralbl Gynakol 124:559. https://doi.org/10.1055/s-2002-40168

    Article  CAS  Google Scholar 

  19. Nnoaham KE, Webster P, Kumbang J, Kennedy SH, Zondervan KT (2012) Is early age at menarche a risk factor for endometriosis? A systematic review and meta-analysis of case-control studies. Fertil Steril 98:702. https://doi.org/10.1016/j.fertnstert.2012.05.035

    Article  Google Scholar 

  20. Papadimitriou A (2016) The evolution of the age at menarche from prehistorical to modern times. J Pediatr Adolesc Gynecol 29:527. https://doi.org/10.1016/j.jpag.2015.12.002

    Article  Google Scholar 

  21. Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP (2003) The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 24:668. https://doi.org/10.1210/er.2002-0019

    Article  Google Scholar 

  22. Magnus MC, Guyatt AL, Lawn RB, Wyss AB, Trajanoska K, Kupers LK et al (2020) Identifying potential causal effects of age at menarche: a Mendelian randomization phenome-wide association study. BMC Med 18:71. https://doi.org/10.1186/s12916-020-01515-y

    Article  Google Scholar 

  23. Hiatt RA, Stewart SL, Hoeft KS, Kushi LH, Windham GC, Biro FM et al (2017) Childhood socioeconomic position and pubertal onset in a cohort of multiethnic girls: implications for breast cancer. Cancer Epidemiol Biomark Prev 26:1714. https://doi.org/10.1158/1055-9965.EPI-17-0496

    Article  Google Scholar 

  24. Deardorff J, Abrams B, Ekwaru JP, Rehkopf DH (2014) Socioeconomic status and age at menarche: an examination of multiple indicators in an ethnically diverse cohort. Ann Epidemiol 24:727. https://doi.org/10.1016/j.annepidem.2014.07.002

    Article  Google Scholar 

  25. Toppari J, Juul A (2010) Trends in puberty timing in humans and environmental modifiers. Mol Cell Endocrinol 324:39. https://doi.org/10.1016/j.mce.2010.03.011

    Article  CAS  Google Scholar 

  26. Fisher MM, Eugster EA (2014) What is in our environment that effects puberty? Reprod Toxicol 44:7. https://doi.org/10.1016/j.reprotox.2013.03.012

    Article  CAS  Google Scholar 

  27. Iavazzo C, Vrachnis N, Gkegkes ID (2022) Peritoneal bacteria contamination and endometriosis pathogenesis. Arch Gynecol Obstet. https://doi.org/10.1007/s00404-022-06467-7

    Article  Google Scholar 

  28. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097. https://doi.org/10.1371/journal.pmed.1000097

    Article  Google Scholar 

  29. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008. https://doi.org/10.1001/jama.283.15.2008

    Article  CAS  Google Scholar 

  30. Burghaus S, Klingsiek P, Fasching PA, Engel A, Haberle L, Strissel PL et al (2011) Risk factors for endometriosis in a German case-control study. Geburtshilfe Frauenheilkd 71:1073. https://doi.org/10.1055/s-0031-1280436

    Article  CAS  Google Scholar 

  31. Mollazadeh S, Sadeghzadeh Oskouei B, Kamalifard M, Mirghafourvand M, Aminisani N, Shobeiri MJ (2019) Association between sexual activity during menstruation and endometriosis: a case-control study. Int J Fertil Steril. 13:230. https://doi.org/10.22074/ijfs.2019.5601

    Article  Google Scholar 

  32. Bouzari Z, Yazdani S, Ahangarkolaee ZH, Zeinalzadeh M, Hajian K (2016) The comparison of menstrual characteristics and BMI in women with endometriosis and without endometriosis. 6:20. https://scientonline.org/open-access/the-comparison-of-menstrual-characteristics-and-bmi-in-women-with-endometriosis-and-without-endometriosis.pdf

  33. Kvaskoff M, Bijon A, Clavel-Chapelon F, Mesrine S, Boutron-Ruault MC (2013) Childhood and adolescent exposures and the risk of endometriosis. Epidemiology 24:261. https://doi.org/10.1097/EDE.0b013e3182806445

    Article  Google Scholar 

  34. Mamdouh HM, Mortada MM, Kharboush IF, Abd-Elateef HA (2011) Epidemiologic determinants of endometriosis among Egyptian women: a hospital-based case-control study. J Egypt Public Health Assoc 86:21. https://doi.org/10.1097/01.EPX.0000395322.91912.56

    Article  Google Scholar 

  35. Saha R, Kuja-Halkola R, Tornvall P, Marions L (2017) Reproductive and lifestyle factors associated with endometriosis in a large cross-sectional population sample. J Womens Health (Larchmt) 26:152. https://doi.org/10.1089/jwh.2016.5795

    Article  Google Scholar 

  36. Treloar SA, Bell TA, Nagle CM, Purdie DM, Green AC (2010) Early menstrual characteristics associated with subsequent diagnosis of endometriosis. Am J Obstet Gynecol 202(534):e1. https://doi.org/10.1016/j.ajog.2009.10.857

    Article  Google Scholar 

  37. Hemmings R, Rivard M, Olive DL, Poliquin-Fleury J, Gagne D, Hugo P et al (2004) Evaluation of risk factors associated with endometriosis. Fertil Steril 81:1513. https://doi.org/10.1016/j.fertnstert.2003.10.038

    Article  Google Scholar 

  38. Flores I, Abreu S, Abac S, Fourquet J, Laboy J, Rios-Bedoya C (2008) Self-reported prevalence of endometriosis and its symptoms among Puerto Rican women. Int J Gynaecol Obstet 100:257. https://doi.org/10.1016/j.ijgo.2007.08.010

    Article  Google Scholar 

  39. Gallagher JS, DiVasta AD, Vitonis AF, Sarda V, Laufer MR, Missmer SA (2018) The impact of endometriosis on quality of life in adolescents. J Adolesc Health 63:766. https://doi.org/10.1016/j.jadohealth.2018.06.027

    Article  Google Scholar 

  40. Johnson CY, Grajewski B, Lawson CC, Whelan EA, Bertke SJ, Tseng CY (2016) Occupational risk factors for endometriosis in a cohort of flight attendants. Scand J Work Environ Health 42:52. https://doi.org/10.5271/sjweh.3538

    Article  Google Scholar 

  41. Matalliotakis IM, Cakmak H, Fragouli YG, Goumenou AG, Mahutte NG, Arici A (2008) Epidemiological characteristics in women with and without endometriosis in the Yale series. Arch Gynecol Obstet 277:389. https://doi.org/10.1007/s00404-007-0479-1

    Article  Google Scholar 

  42. Missmer SA, Hankinson SE, Spiegelman D, Barbieri RL, Malspeis S, Willett WC et al (2004) Reproductive history and endometriosis among premenopausal women. Obstet Gynecol 104:965. https://doi.org/10.1097/01.AOG.0000142714.54857.f8

    Article  Google Scholar 

  43. Templeman C, Marshall SF, Ursin G, Horn-Ross PL, Clarke CA, Allen M et al (2008) Adenomyosis and endometriosis in the California Teachers Study. Fertil Steril 90:415. https://doi.org/10.1016/j.fertnstert.2007.06.027

    Article  Google Scholar 

  44. Buck Louis GM, Hediger ML, Pena JB (2007) Intrauterine exposures and risk of endometriosis. Hum Reprod 22:3232. https://doi.org/10.1093/humrep/dem338

    Article  Google Scholar 

  45. Deeks JJ (2001) Systematic reviews of evaluations of diagnostic and screening tests. BMJ 323:157

    Article  CAS  Google Scholar 

  46. Sterne JA, Egger M (2001) Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol 54:1046. https://doi.org/10.1016/s0895-4356(01)00377-8

    Article  CAS  Google Scholar 

  47. Lin L, Chu H (2018) Quantifying publication bias in meta-analysis. Biometrics 74:785. https://doi.org/10.1111/biom.12817

    Article  Google Scholar 

  48. Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088

    Article  CAS  Google Scholar 

  49. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629. https://doi.org/10.1136/bmj.315.7109.629

    Article  CAS  Google Scholar 

  50. Vigano P, Somigliana E, Panina P, Rabellotti E, Vercellini P, Candiani M (2012) Principles of phenomics in endometriosis. Hum Reprod Update 18:248. https://doi.org/10.1093/humupd/dms001

    Article  CAS  Google Scholar 

  51. Sampson JA (1927) Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol 3:93

    CAS  Google Scholar 

  52. Marcellin L, Santulli P, Pinzauti S, Bourdon M, Lamau MC, Borghese B et al (2019) Age at menarche does not correlate with the endometriosis phenotype. PLoS ONE 14:e0219497. https://doi.org/10.1371/journal.pone.0219497

    Article  CAS  Google Scholar 

  53. Herman-Giddens ME (2006) Recent data on pubertal milestones in United States children: the secular trend toward earlier development. Int J Androl 29:241. https://doi.org/10.1111/j.1365-2605.2005.00575.x

    Article  Google Scholar 

  54. Piekarski DJ, Johnson CM, Boivin JR, Thomas AW, Lin WC, Delevich K et al (2017) Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? Brain Res 1654:123. https://doi.org/10.1016/j.brainres.2016.08.042

    Article  CAS  Google Scholar 

  55. Anderson SE, Must A (2005) Interpreting the continued decline in the average age at menarche: results from two nationally representative surveys of U.S. girls studied 10 years apart. J Pediatr 147:753. https://doi.org/10.1016/j.jpeds.2005.07.016

    Article  Google Scholar 

  56. Bougie O, Yap MI, Sikora L, Flaxman T, Singh S (2019) Influence of race/ethnicity on prevalence and presentation of endometriosis: a systematic review and meta-analysis. BJOG 126:1104. https://doi.org/10.1111/1471-0528.15692

    Article  CAS  Google Scholar 

  57. Cramer DW, Missmer SA (2002) The epidemiology of endometriosis. Ann N Y Acad Sci 955:11. https://doi.org/10.1111/j.1749-6632.2002.tb02761.x

    Article  Google Scholar 

  58. Pierce MB, Leon DA (2005) Age at menarche and adult BMI in the Aberdeen children of the 1950s cohort study. Am J Clin Nutr 82:733. https://doi.org/10.1093/ajcn/82.4.733

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by Research Foundation of Shenzhen Baoan Women’s and Children’s Hospital, Jinan University to BL (BAFY 2020005).

Author information

Authors and Affiliations

  1. Department of Biobank, Shenzhen Baoan Women’s and Children’s Hospital, Jinan University, Guangdong, 518102, China

    Mei-Yin Lu, Jia-Li Niu & Bin Liu

Authors
  1. Mei-Yin Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jia-Li Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MYL: data collection, data analysis, and manuscript writing. JLN: data collection and data analysis. BL: protocol/project development and manuscript writing/editing.

Corresponding author

Correspondence to Bin Liu.

Ethics declarations

Conflict of interests

The authors have no conflicts of interest to declare.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

This manuscript is approved by all the authors for publication.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

404_2022_6541_MOESM1_ESM.jpg

Supplementary file1 Linear analysis between NOS score and log(OR) for 16 included studies. NOS, Newcastle-Ottawa scale. Circle size means the reported OR and its 95% CI. Red Line and grey band means the predicted OR and its 95% CI (JPG 92 KB)

404_2022_6541_MOESM2_ESM.jpg

Supplementary file2 Meta-analysis of included studies presented by the subgroups of study countries: Asia & Africa vs. Europe & Oceania vs. North America (JPG 199 KB)

404_2022_6541_MOESM3_ESM.jpg

Supplementary file3 Meta-analysis of included studies presented by the subgroups of study area: low-income countries vs. others (JPG 172 KB)

404_2022_6541_MOESM4_ESM.jpg

Supplementary file4 Meta-analysis of included studies presented by the subgroups of study type: Case-control studies vs. Cohort studies (JPG 174 KB)

404_2022_6541_MOESM5_ESM.jpg

Supplementary file5 Meta-analysis of included studies presented by the subgroups of NOS score: ≤5 vs. >5. NOS, Newcastle-Ottawa scale (JPG 181 KB)

404_2022_6541_MOESM6_ESM.png

Supplementary file6 Funnel plot of the publication bias in this meta-analyses. (A)Funnel plot with pseudo 95% CI of 16 included studies. (B), Begg’s test for small-study effects (PNG 88 KB)

Supplementary file7 Egger's test for 16 included studies in this meta-analysis (PNG 62 KB)

Supplementary file8 Sensitivity analysis of 16 included studies in this meta-analysis (JPG 205 KB)

404_2022_6541_MOESM9_ESM.jpg

Supplementary file9 Forest plot of the association between early menarche and endometriosis in studies with different quality on the ascertainment of exposure (age at menarche): 2(top), studies with poor quality on the ascertainment of exposure. 1(bottom), and studies with higher quality on the ascertainment of exposure (JPG 179 KB)

404_2022_6541_MOESM10_ESM.jpg

Supplementary file10 Forest plot of the association between early menarche and endometriosis in 13 included studies, when removing 3 studies with inadequately controlled for potential confounders (JPG 164 KB)

Supplementary file11 Quality of included studies using Newcastle-Ottawa scale (PPTX 70 KB)

Supplementary file12 (DOC 48 KB)

Supplementary file13 (DOC 58 KB)

Appendix

Appendix

  1. A.

    PRISMA 2009 CHECKLIST Online Supplementary Material.

  2. B.

    MOOSE CHECKLIST Online Supplementary Material.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lu, MY., Niu, JL. & Liu, B. The risk of endometriosis by early menarche is recently increased: a meta-analysis of literature published from 2000 to 2020. Arch Gynecol Obstet 307, 59–69 (2023). https://doi.org/10.1007/s00404-022-06541-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00404-022-06541-0

Keywords

Search

Navigation