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Low AMH- Is it linked to Infertility?

Oration delivered by Dr Sujoy Dasgupta at Yuvacon, conference organized by the BOGS (Bengal Obstetric and Gynaecological Society) held on 22-23 April, 2023

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Low AMH-
Is it related to Infertility?
Dr Sujoy Dasgupta
MBBS (Gold Medalist, Hons)
MS (OBGY- Gold Medalist)
DNB (New Delhi)
MRCOG (London)
Advanced ART Course for Clinicians (NUHS, Singapore)
M Sc, Sexual and Reproductive Medicine (South Wales, UK)
Consultant: Reproductive Medicine, Genome Fertility Centre, Kolkata
Managing Committee Member, BOGS, 2022-23
Executive Committee Member, ISAR Bengal, 2022-24
Clinical Examiner, MRCOG Part 3 Examination
Winner, Prof Geoffrey Chamberlain Award, RCOG World Congress, London, 2019
Declining ovarian reserve is THE RULE
Declining ovarian reserve is THE RULE
Terminology
1. Ovarian Reserve- Quantity and quality of
remaining oocytes present in both the ovaries
at a given age
2. Ovarian Responsiveness- Number of oocytes
developed/ retrieved after COH
3. Ovarian Ageing- Decline in quantity and
quality of ovarian activity because of
individualized rhythm of the “biological
clock”
Ovarian Reserve Tests
Commonly Used
• Age
• AMH
• AFC
• FSH
Others
• Inhibin B
• Ovarian Volume
• Ovarian blood flow
(Doppler)
• Dynamic Tests
Female Age-
Most valuable parameter

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Low AMH- Is it linked to Infertility?

  • 1. Low AMH- Is it related to Infertility? Dr Sujoy Dasgupta MBBS (Gold Medalist, Hons) MS (OBGY- Gold Medalist) DNB (New Delhi) MRCOG (London) Advanced ART Course for Clinicians (NUHS, Singapore) M Sc, Sexual and Reproductive Medicine (South Wales, UK) Consultant: Reproductive Medicine, Genome Fertility Centre, Kolkata Managing Committee Member, BOGS, 2022-23 Executive Committee Member, ISAR Bengal, 2022-24 Clinical Examiner, MRCOG Part 3 Examination Winner, Prof Geoffrey Chamberlain Award, RCOG World Congress, London, 2019
  • 4. Terminology 1. Ovarian Reserve- Quantity and quality of remaining oocytes present in both the ovaries at a given age 2. Ovarian Responsiveness- Number of oocytes developed/ retrieved after COH 3. Ovarian Ageing- Decline in quantity and quality of ovarian activity because of individualized rhythm of the “biological clock”
  • 5. Ovarian Reserve Tests Commonly Used • Age • AMH • AFC • FSH Others • Inhibin B • Ovarian Volume • Ovarian blood flow (Doppler) • Dynamic Tests
  • 7. Day3 FSH FSH >15 IU/L + Estradiol >75 pg/ml (>200 pmol/L) • Cycle dependent • Inter-cycle variation • Single abnormal FSH- not reliable <40 yr of age
  • 8. Antral Follicle Count (AFC) • Day 2-4 • TVS- 2-9 mm follicles • Direct measure of cohort of follicles capable of responding to the stimulation • Observer and machine dependent • 3-D manual and sono- AVC- ? • Problematic in presence of ovarian mass
  • 9. Anti-Műllerian Hormone (AMH) • Secreted by granulosa cells • Paracrine control, independent of HPO endocrine feedback • Correlates with AFC, FSH, Inhibin B, E2 • Higher sensitivity and specificity than conventional markers • Declines earlier than FSH rise
  • 10. Primordial Follicle Small Preantral Large Preantral Small Antral (2-7 mm) Large Antral (8-12 mm) Preovulatory Atresia Atresia Atresia AMH FSH 70-80 days Last 20 days Initial Recruitment Cycle Recruitment Selection Dominance Paracrine Control (Gn Independent) Endocrine Control (Gn Dependent) Estrogen
  • 11. Role of AMH in Ovarian Dynamics • Prevention of unnecessary and excessive recruitment of primordial follicles • Restriction of follicular sensitivity to FSH • Follicular Preservation • Indirectly helping mono-follicular development
  • 12. Variability of AMH La Marca A, Grisendi V, Griesinger G. How Much Does AMH Really Vary in Normal Women? Int J Endocrinol. 2013;2013:959487.
  • 13. Intra-Class Coefficient (ICC) Fanchin R, Taieb J, Lozano DH, Ducot B, Frydman, R, Bouyer J. High reproducibility of serum anti-Mullerian hormone measurements suggests a multistaged follicular secretion and strengthens its role in the assessment of ovarian follicular status. Hum Reprod 2005; 20(4): 923–7.
  • 15. Reproductive and lifestyle factors affecting AMH • Direct association of low AMH 1. Increasing age 2. Short cycles/ Amenorrhea 3. Family history of POF. • No correlation with 1. Smoking 2. Sleep 3. Diet 4. BMI 5. Sedentary lifestyle 6. Cell phone or laptop use Banerjee K, Thind A, Bhatnagar N, Singla B, Agria K, Bajaj P, Jindal A, Arora S, Goyal P, Mittal B, Malhotra K, Pai H, Malhotra J, Goel P, Jindal N. Effect of Reproductive and Lifestyle Factors on Anti-Mullerian Hormone Levels in Women of Indian Origin. J Hum Reprod Sci. 2022 Jul-Sep;15(3):259-271.
  • 16. How “low” is “low”? • No unanimous consensus Alipour, F.G., Rasekhjahromi, A., Maalhagh, M., Sobhanian, S., & Hosseinpoor, M. Comparison of Specificity and Sensitivity of AMH and FSH in Diagnosis of Premature Ovarian Failure. Disease Markers, 2015;2015:585604.
  • 17. Doroftei B, Mambet C, Zlei M. It's Never over until It's over: How Can Age and Ovarian Reserve Be Mathematically Bound through the Measurement of Serum AMH- A Study of 5069 Romanian Women. PLoS One. 2015 Apr 24;10(4):e0125216.
  • 18. Rate of decline in AMH Age (year) Mean decline Median decline Standard deviation decline <30 0.3 ng/ml/year 0.25 ng/ml/year 0.15 ng/ml/year 31-35 0.2 ng/ml/year 0.2 ng/ml/year 0.15 ng/ml/year >36 0.1 ng/ml/year 0.1 ng/ml/year 0.1 ng/ml/year Doroftei B, Mambet C, Zlei M. It's Never over until It's over: How Can Age and Ovarian Reserve Be Mathematically Bound through the Measurement of Serum AMH- A Study of 5069 Romanian Women. PLoS One. 2015 Apr 24;10(4):e0125216.
  • 19. Discordance between ovarian reserve tests • Approximately 1/5 patients in clinical practice had discordance in their AFCs and AMH levels (Zhang et al., Reprod Bio Online, 2019) • Laboratory vs Machine? • Intermediate prognosis
  • 20. AMH is assay-dependent Li HWR, Robertson DM, Burns C, Ledger WL. Challenges in Measuring AMH in the Clinical Setting. Front Endocrinol (Lausanne). 2021 May 24;12:691432.
  • 21. AFC vs AMH • The faster decline in AMH than in AFC with age • The reproducibility for AMH seemed much better than for AFC. Arvis P, Rongières C, Pirrello O, Lehert P. Reliability of AMH and AFC measurements and their correlation: a large multicenter study. J Assist Reprod Genet. 2022 May;39(5):1045-1053.
  • 22. AMH vs AFC- Evidence from Endometrioma Surgery Younis JS, Shapso N, Ben-Sira Y, Nelson SM, Izhaki I. Endometrioma surgery-a systematic review and meta-analysis of the effect on antral follicle count and anti- Müllerian hormone. Am J Obstet Gynecol. 2022 Jan;226(1):33-51.e7.
  • 23. Zhang Y, Xu Y, Xue Q, Shang J, Yang X, Shan X, Kuai Y, Wang S, Zeng C. Discordance between antral follicle counts and anti-Müllerian hormone levels in women undergoing in vitro fertilization. Reprod Biol Endocrinol. 2019 Jul 4;17(1):51. AFC AMH Cycle cancellation rate Clinical pregnancy rate Group A ≥7 ≥1.1 ng/ml 33.88% 43.32% Group B ≥7 <1 ng/ml 32.94% 43.86% Group C <7 ≥1.1 ng/ml 46.61% 23.81% Group D <7 <1 ng/ml 68.73% 25% AFC better than AMH for predicting POR
  • 24. Ovarian Reserve Quantitative • Poor response to COH Qualitative • No test can predict • Age
  • 26. Age and Euploidy Capalbo A et al.. Hum Reprod Update 2017; 23:706–722.
  • 27. Does low AMH mean infertility? • Prospective, time-to-pregnancy cohort study of women (N=981) 30–44 years, trying to conceive for ≤3 months • Raleigh-Durham area, North Carolina Steiner AZ, Pritchard D, Stanczyk FZ, Kesner JS, Meadows JW, Herring AH, Baird DD. Association Between Biomarkers of Ovarian Reserve and Infertility Among Older Women of Reproductive Age. JAMA. 2017 Oct 10;318(14):1367-1376.
  • 28. AMH is NOT the marker for “natural fertility” Steiner AZ, Pritchard D, Stanczyk FZ, Kesner JS, Meadows JW, Herring AH, Baird DD. Association Between Biomarkers of Ovarian Reserve and Infertility Among Older Women of Reproductive Age. JAMA. 2017 Oct 10;318(14):1367-1376.
  • 29. 41 yr, undetectable AMH !!! Fraisse T, Ibecheole V, Streuli I, Bischof P, de Ziegler D. Undetectable serum anti-Müllerian hormone levels and occurrence of ongoing pregnancy. Fertil Steril. 2008 Mar;89(3):723.e9-11
  • 30. Low AMH ≠ Donor oocyte • The predictive accuracy of AMH for 1-year CLBR in GnRH antagonist treatment cycles was limited and did NOT yield much additional value on top of age. • Withholding treatment based on predictors such as age, AMH, or combination, remains problematic. Hamdine O, Eijkemans MJ, Lentjes EW, Torrance HL, Macklon NS, Fauser BC, Broekmans FJ. Antimüllerian hormone: Prediction of cumulative live birth in gonadotropin-releasing hormone antagonist treatment for in vitro fertilization. Fertil Steril 2015; 104: 891–8.
  • 31. Predictive power of AMH • Broer SL, van Disseldorp J, Broeze KA, Dolleman M, Opmeer BC, Bossuyt P, Eijkemans MJ, Mol BW, Broekmans FJ; IMPORT study group. Added value of ovarian reserve testing on patient characteristics in the prediction of ovarian response and ongoing pregnancy: an individual patient data approach. Hum Reprod Update. 2013 Jan-Feb;19(1):26-36.
  • 32. AMH can predict ovarian response
  • 33. IVF is stressful for Fertility Physicians
  • 34. Low AMH in younger women • Retrospective cohort study • Only patients <38 years old at time oocyte retrieval • Patients with AMH values in bottom 10th %tile were compared to patients in the IQR (25–75th %tile). Morin SJ, Patounakis G, Juneau CR, Neal SA, Scott RT, Seli E. Diminished ovarian reserve and poor response to stimulation in patients <38 years old: a quantitative but not qualitative reduction in performance. Hum Reprod. 2018 Aug 1;33(8):1489-1498.
  • 35. Morin SJ, Patounakis G, Juneau CR, Neal SA, Scott RT, Seli E. Diminished ovarian reserve and poor response to stimulation in patients <38 years old: a quantitative but not qualitative reduction in performance. Hum Reprod. 2018 Aug 1;33(8):1489-1498.
  • 36. Low AMH in older women • Retrospectively analysed • Women aged >36 years • Divided into two groups: 1. AMH high (= > 1.1 ng/ml, H) 2. AMH low (< 1.1 ng/ml, L) Dai X, Wang Y, Yang H, Gao T, Yu C, Cao F, Xia X, Wu J, Zhou X, Chen L. AMH has no role in predicting oocyte quality in women with advanced age undergoing IVF/ICSI cycles. Sci Rep. 2020 Nov 12;10(1):19750.
  • 37. Age rather than AMH affects the quality of oocytes in older women Dai X, Wang Y, Yang H, Gao T, Yu C, Cao F, Xia X, Wu J, Zhou X, Chen L. AMH has no role in predicting oocyte quality in women with advanced age undergoing IVF/ICSI cycles. Sci Rep. 2020 Nov 12;10(1):19750.
  • 38. Low AMH- Young vs Older • 296 infertile patients with AMH measured • Younger group, aged 25-38 years • Older group, aged 39-42 years • AMH levels of <1.0ng/mL and ≥1.0ng/mL were compared. • Young women with low AMH- good prognosis if blastocyst can be developed Miyagi M, Mekaru K, Nakamura R, Oishi S, Akamine K, Heshiki C, Aoki Y. Live birth outcomes from IVF treatments in younger patients with low AMH. JBRAAssist Reprod. 2021 Jul 21;25(3):417-421.
  • 39. AMH is a predictor of live birth among older, but not younger, women Miyagi M, Mekaru K, Nakamura R, Oishi S, Akamine K, Heshiki C, Aoki Y. Live birth outcomes from IVF treatments in younger patients with low AMH. JBRAAssist Reprod. 2021 Jul 21;25(3):417-421.
  • 42. • A young woman with a poor response >>> older woman with a poor response Poor Responders ≠ Same Oudendijk JF, Yarde F, Eijkemans MJ, Broekmans FJ, Broer SL. The poor responder in IVF: is the prognosis always poor?: a systematic review. Hum Reprod Update. 2012 Jan-Feb;18(1):1-11. doi: 10.1093/humupd/dmr037. Epub 2011 Oct 10. PMID: 21987525.
  • 43. ESHRE Bologna: One size does NOT fit for all
  • 44. Poseidon (Patient-Oriented Strategies Encompassing IndividualizeD Oocyte Number)
  • 46. Young women Older women Good Ovarian Reserve Group 1 Group 2 Poor Ovarian Reserve Group 3 Group 4
  • 47. Good Ovarian Reserve Group 1 Group 2 Poor Ovarian Reserve Group 3 Group 4 Unexpected poor response Expected poor response •Asynchrony •Gn Receptor gene polymorphism •Low dose Gn (like high BMI) •Less potent Gn •Unexplained •Ovarian aging •Ovarian insult (surgery) •Genetic (Karyo, FMR1)
  • 48. Young women Older women Good Ovarian Reserve Group 1 Group 2 Poor Ovarian Reserve Group 3 Group 4 Low risk of Aneuploidy High risk of Aneuploidy
  • 49. CLBR depends on POSEIDON group
  • 50. Stimulation regimes for POR High dose Gn No benefits >300 IU FSH GnRH Agonist protocols Long protocol Oversuppression Short protocol (Flare-up) Theoretically less suppression Microdose flare up protocol Cost-friendly Ultra-short protocol Not much benefit Cessation/ Stop protocol No additional advantage GnRH Antagonist protocols Flexible vs fixed protocol Most widely used GnRH Agonist-antagonist protocol Not much benefit Natural cycle Not recommended Modified natural cycle Not recommended Mild stimulation protocol CC/ letrozole + Gn + Antag No additional benefit Luteal phase stimulation No additional benefit Dual stimulation Needs further studies
  • 51. Does low AMH mean increased risk of pregnancy loss?
  • 52. Serum AMH- a marker of RPL? • RPL patients demonstrated AMH levels significantly lower than the normal population, both in women aged ≤35 years (p<0.004), and those aged >35 years (p>0.03). Catherine D. McCormack, Shalem Y. Leemaqz, Denise L. Furness, Gustaaf A. Dekker & Claire T. Roberts (2019) Anti-Müllerian hormone levels in recurrent embryonic miscarriage patients are frequently abnormal, and may affect pregnancy outcomes, Journal of Obstetrics and Gynaecology, 39:5, 623-627
  • 53. Low AMH does NOT increase risk of pregnancy loss after IVF-ICSI • Retrospective cohort study on 1383 women undergoing their first IVF/ICSI cycle in Finland Peuranpää P, Hautamäki H, Halttunen-Nieminen M, Hydén-Granskog C, Tiitinen A. Low anti-Müllerian hormone level is not a risk factor for early pregnancy loss in IVF/ICSI treatment. Hum Reprod. 2020 Mar 27;35(3):504-515.
  • 54. Low AMH was associated with embryo aneuploidy ONLY ≥35 years age • Retrospective study of 422 IVF cycles of 394 unexplained RPL patients undergoing PGT-A, • Divided on AMH levels 1. Group 1: low AMH <1.50 ng/ml 2. Group 2: normal AMH 1.50– < 5.60 ng/ml 3. Group 3: high AMH ≥ 5.60 ng/ml • Aneuploidy was significantly higher in the low AMH group compared with that in the normal AMH group (P1vs2 = 0.002) and high AMH group (P1vs3 = 0.015). • After age stratification, embryonic aneuploidy rate was still significantly different among AMH groups with a similar trend in women ≥35 years old (P1vs2 = 0.025, P1vs3 = 0.035), but not in young subjects Jiang X, Yan J, Sheng Y, Sun M, Cui L, Chen ZJ. Low anti-Müllerian hormone concentration is associated with increased risk of embryonic aneuploidy in women of advanced age. Reprod Biomed Online. 2018 Aug;37(2):178-183.
  • 55. Why we should NOT ignore low AMH?
  • 56. AMH- earlier predictor of POF AMH Day3 FSH Sensitivity 80% 29% Specificity 79% 79% PPV 17% 17% NPV 99% 87% Diagnostic accuracy 79% 72% Alipour, F.G., Rasekhjahromi, A., Maalhagh, M., Sobhanian, S., & Hosseinpoor, M. Comparison of Specificity and Sensitivity of AMH and FSH in Diagnosis of Premature Ovarian Failure. Disease Markers, 2015;2015:585604.
  • 57. AMH is highly predictive for timing of menopause Broer SL, Eijkemans MJ, Scheffer GJ, van Rooij IA, de Vet A, Themmen AP, Laven JS, de Jong FH, Te Velde ER, Fauser BC, Broekmans FJ. Anti-mullerian hormone predicts menopause: a long-term follow-up study in normoovulatory women. J Clin Endocrinol Metab. 2011 Aug;96(8):2532-9
  • 58. Fixed interval hypothesis Broekmans FJ, Soules MR, Fauser BC. Ovarian aging: mechanisms and clinical consequences. Endocr Rev. 2009 Aug;30(5):465-93.
  • 59. AMH can help in decision taking
  • 60. See the overall scenario • Age • Duration of trying for pregnancy • Previous treatment received • Tubal factor • Male factor • Other pathologies- endometriosis, fibroid, hydrosalpinx etc • What the couple wants
  • 61. Low AMH and ……….. Tube block in HSG • IVF rather than laparoscopy Tube, semen normal • Unexplained subfertility (ASRM, 2020) Male factor • Not to do repeated IUI cycles
  • 63. Endometriosis- the biggest confusion • In endometriosis, with and without a history of ovarian surgery, ovarian reserve markers were worse (lower AMH and higher FSH) compared to women with male factors Romanski PA, Brady PC, Farland LV, Thomas AM, Hornstein MD. The effect of endometriosis on the antimüllerian hormone level in the infertile population. J Assist Reprod Genet. 2019 Jun;36(6):1179-1184.
  • 64. Endometrioma-related reduction in ovarian reserve (ERROR) Kasapoglu I, Ata B, Uyaniklar O, Seyhan A, Orhan A, Yildiz Oguz S, Uncu G. Endometrioma-related reduction in ovarian reserve (ERROR): a prospective longitudinal study. Fertil Steril. 2018 Jul 1;110(1):122-127.
  • 65. Endometriosis- surgery or not Yılmaz Hanege B, Güler Çekıç S, Ata B. Endometrioma and ovarian reserve: effects of endometriomata per se and its surgical treatment on the ovarian reserve. Facts Views Vis Obgyn. 2019 Jun;11(2):151-157.
  • 67. • In women identified as poor responders undergoing ART, pre-treatment with DHEA or testosterone may be associated with improved live birth rates. • The overall quality of the evidence is moderate. • There is insufficient evidence to draw any conclusions about the safety of either androgen. • Definitive conclusions regarding the clinical role of either androgen awaits evidence from further well-designed studies. Role of DHEA Nagels HE, Rishworth JR, Siristatidis CS, Kroon B. Androgens (dehydroepiandrosterone or testosterone) for women undergoing assisted reproduction. Cochrane Database Syst Rev. 2015 Nov 26;(11):CD009749
  • 70. Unanswered questions? • ICSI for all ? • Ideal day of transfer- D3/D5? • PGT for all? • Oocyte pooling and embryo banking? • In vitro activation of oocytes (IVA) • Mitochondrial transfer • Intraovarian PRP
  • 71. Social egg freezing- race against time? • Often perceived (and promoted) as a form of insurance • Success rates will be limited in women who are already in their mid–late 30s • Significant costs • Low fecundity rate
  • 72. Donor oocyte • Repeated IVF failure • High FSH and low AMH ( how high is high and how low is low) • Counselling
  • 73. Conclusion • AMH predicts ovarian response • AMH can help in decision making • AMH cannot predict egg quality, pregnancy, live birth • Low AMH ≠ Egg donation • Low AMH ≠ IVF • See the overall scenario • Can offer adjuvant (DHEA) but do NOT delay active treatment • Best stimulation protocol? • Unconventional protocols in IVF need further studies • Overall prognosis may be guarded for low AMH + age >35
  • 74. AMH is a number

Editor's Notes

  1. The ICC is the ratio of the interindividual variability over the total variability. Hence the higher the ICC, the lower the intraindividual variability. Both studies concluded that 89% of the variation in AMH was due to between-subject variation, while only 11% of variability was secondary to individual fluctuation in AMH levels (Figure 4).
  2. Figure 1 Patients with precycle AMH levels <10th percentile have lower oocyte yields than those in the 25–75th percentile. However, on mixed effects model, a successfully fertilized oocyte derived from a patient with AMH in the <10th percentile has the same odds of forming a quality blastocyst, being euploid and producing a live birth after transfer of an euploid blastocyst. Unless provided in the caption above, the following copyright applies to the content of this slide: © The Author(s) 2018. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.comThis article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)
  3. | Poseidon criteria of low prognosis patients in ART. Four distinct groups of low prognosis patients can be established based on quantitative and qualitative parameters, namely: 1. The age of the patient and the expected embryo aneuploidy rate; 2. Ovarian biomarkers (antral follicle count [AFC] and/or anti-Müllerian hormone [AMH]), and 3. The ovarian response of the patient in terms of oocyte quantity provided a previous cycle of stimulation was carried out. Art drawing by Chloé Xilinas, EXCEMED, Rome, Italy. Adapted from Esteves et al