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Anti-Müllerian Hormone in African-American Women With Reproductive health and APS Lupus Sci Med: first published as 10.1136/lupus-2020-000439 on 1 November 2020. Downloaded from Anti- Müllerian hormone in African- American women with systemic lupus erythematosus Meghan Angley ,1 Jessica B Spencer,2 S Sam Lim ,1,3 Penelope P Howards1 To cite: Angley M, Spencer JB, ABSTRACT organs include the skin, musculoskeletal Lim SS, et al. Anti- Müllerian Objective Women with SLE may experience ovarian system, and heart. In women, organ damage hormone in African- American insufficiency or dysfunction due to treatment or disease can also manifest as ovarian insufficiency or women with systemic effects. Anti- Müllerian hormone (AMH), a marker of ovarian lupus erythematosus. dysfunction. reserve, has been examined in small populations of women Lupus Science & Medicine Anti- Müllerian hormone (AMH) is a with SLE with conflicting results. To date, these studies 2020;7:e000439. doi:10.1136/ marker of ovarian reserve. Unlike follicle- lupus-2020-000439 have included very few African- American women, the racial/ethnic group at greatest risk of SLE. stimulating hormone, AMH levels remain Methods We enrolled African- American women aged 22– relatively constant throughout a woman’s Received 20 August 2020 40 years diagnosed with SLE after age 17 from the Atlanta menstrual cycle so they can be measured at Revised 18 September 2020 Metropolitan area. Women without SLE from the same any point during the menstrual cycle. AMH Accepted 1 October 2020 area were recruited from a marketing list for comparison. is a hormone secreted by granulosa cells of AMH was measured in serum using the Ansh Labs assay small antral follicles and correlates with the (Webster, Texas, USA). We considered AMH levels <1.0 ng/ number of developing follicles in the ovaries. mL and AMH <25th percentile of comparison women as separate dichotomous outcomes. Log- binomial regression It is a marker of ovarian reserve and therefore models estimating prevalence ratios were adjusted for age, declines throughout a woman’s reproductive 5 body mass index and hormonal contraception use in the lifespan. AMH has clinical utility as an indi- previous year. cator of a woman’s response to ovarian stimu- Results Our sample included 83 comparison women lation for in vitro fertilisation.6 Several studies without SLE, 68 women with SLE and no history of have also found AMH to be somewhat predic- cyclophosphamide (SLE/CYC−) and 11 women with tive of time- to- menopause.7–9 SLE and a history of cyclophosphamide treatment (SLE/ AMH has been examined in women with http://lupus.bmj.com/ CYC+). SLE/CYC+ women had a greater prevalence of AMH <1.0 ng/mL compared with women without SLE SLE in several studies, but with conflicting (prevalence ratio (PR): 2.90, 95% CI: 1.29 to 6.51). SLE/ results. Generally, there is a consensus that CYC− women were also slightly more likely to have AMH is lower among women with SLE treated AMH <1.0 ng/mL (PR: 1.62, 95% CI: 0.93 to 2.82) than with cyclophosphamide (CYC).10–13 However, comparison women. Results were similar when considering while some found a substantial difference AMH <25th percentile by age of comparison women. in AMH levels between women with SLE © Author(s) (or their Conclusions Treatment with CYC is associated with low not treated with CYC and women without on September 28, 2021 by guest. Protected copyright. employer(s)) 2020. Re- use AMH in African-American women with SLE. SLE itself SLE,14–16 others did not.10 17 Overall, these permitted under CC BY. may also be associated with reduced AMH, but to a lesser Published by BMJ. extent. studies have varying limitations. Most include 1Department of Epidemiology, fewer than 50 women with SLE and some lack Rollins School of Public Health, comparison groups of women without SLE. Emory University, Atlanta, The largest study included 112 women with Georgia, USA 2Division of Reproductive INTRODUCTION SLE, but did not include a comparison group Endocrinology and Infertility, SLE is an autoimmune disease affecting of women without SLE and instead compared Department of Gynecology and multiple organ systems. SLE is nine times women who had been treated with CYC with Obstetrics, Emory University more common among women, and it is women with SLE who had never been treated School of Medicine, Atlanta, 12 primarily diagnosed during women’s repro- with CYC. One study did not distinguish Georgia, USA 1 3Department of Medicine, ductive years. SLE is characterised by periods between women with SLE who had been 18 Division of Rheumatology, Emory of quiescence and flares where the disease treated with CYC and those that had not. In University School of Medicine, may be highly active.2 It is also associated addition, while 10% of the study population in Atlanta, Georgia, USA with the potential for progressive, irreversible the study by Marder et al was classified as ‘non- 3 Correspondence to organ damage. Over half of patients with white’, no studies specifically examine AMH Ms Meghan Angley; mangley@ SLE show at least some organ damage after among African- American or black women emory. edu 5 years of the disease.4 Commonly affected with SLE.13 In the USA, African-American Angley M, et al. Lupus Science & Medicine 2020;7:e000439. doi:10.1136/lupus-2020-000439 1 Lupus Science & Medicine Lupus Sci Med: first published as 10.1136/lupus-2020-000439 on 1 November 2020. Downloaded from women are at 3 times the risk of SLE compared with African- American participants in the pilot study (89% of white women and also tend to experience more severe participants). SLE, potentially causing greater ovarian toxicity.19–21 Data on comparison women were obtained from the Thus, the relationship between SLE and ovarian reserve Furthering Understanding of Cancer, Health and Survi- as measured by AMH may differ among African-American vorship in Adult (FUCHSIA) Women’s Study.23 Compar- women. ison women in the FUCHSIA Women’s Study were In this analysis, we examined AMH levels in a sample originally recruited from marketing lists to serve as the of African- American women with SLE, compared with general population comparison for female cancer survi- African- American women without SLE. We distinguished vors. We restricted the FUCHSIA Women’s Study compar- between women with SLE who had a history of CYC ison group to women 22–40 years of age, who had never treatment and women with SLE who had never been had a hysterectomy, and who lived in the metropolitan treated with CYC. We hypothesised that women with SLE Atlanta area at the time of the interview to make them would have lower AMH than women without SLE after comparable to the women with SLE enrolled in the LIFE controlling for age, and that women with a history of study. The comparison women completed an interview treatment with CYC would have the lowest AMH levels. similar to the one used in the LIFE study and provided oral consent at the time of interview. A subset of the comparison women in FUCHSIA completed clinic visits where they provided blood samples and their height and METHODS weight were measured by study staff. Study participants Among both the SLE and the comparison women, we Women with SLE were enrolled from the Georgians Organ- excluded those with a self-reported history of polycystic ized Against Lupus (GOAL) Cohort, an ongoing cohort ovarian syndrome (PCOS). Women with PCOS typically of patients with validated cases of SLE from the Atlanta have very high AMH levels which may skew interpreta- metropolitan area. The primary source of recruited tion for the rest of the sample.5 We defined hormonal participants for GOAL was the Georgia Lupus Registry contraception use in the past year as use of oral contra- (GLR), a population-based registry of all SLE cases in ceptive pills, the patch, the NuvaRing, Depo- Provera or 20 Fulton and DeKalb counties in Georgia. Additional the subdermal implant in the previous 12 months, but patients in GOAL were enrolled from Emory Healthcare, excluded the hormonal intrauterine device. We created Grady Memorial Hospital and diverse community rheu- three exposure categories: women with SLE with no matology clinics. The case definition of SLE was meeting history of CYC treatment (SLE/CYC−), women with at least four of the American College of Rheumatology SLE who had been treated with CYC (SLE/CYC+) and 22 (ACR) Classification criteria for SLE (GLR, GOAL) or comparison women. meeting three ACR criteria with a final diagnosis of SLE by a board- certified rheumatologist (GLR). Patient and public involvement http://lupus.bmj.com/ One hundred women were recruited from GOAL for Patients were not involved in the design or analysis of this the Lupus Impacting the Female Experience (LIFE) study. Study, a pilot study examining women’s reproductive AMH assay and fertility histories while living with SLE. Women were Serum AMH was measured among women in LIFE and recruited by phone and email notices and in person at FUCHSIA using the same ELISA (UltraSensitive AMH/ lupus clinics at Emory Healthcare and Grady Memorial MIS ELISA, Ansh Labs, Webster, Texas, USA). Age at on September 28, 2021 by guest. Protected copyright. Hospital. Eligible women were aged 22–40 years at the interview is the same age at which AMH was measured. time of enrolment and had been diagnosed with SLE at Serum AMH was measured in duplicate and samples were age 18–35 years. Since part of the study objectives were to processed by the University of Southern California Repro- examine women’s reproductive goals, we restricted enrol- ductive Endocrinology Laboratory. The limit of detection ment to women who were more likely to be potentially (LOD) of the assay was 0.076 ng/mL.
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