The ovarian reserve of patients with systemic lupus erythematosus (SLE) may be affected by disease activity and medication use. Studies have found that patients with SLE have similar fertility rates as healthy women of the same age. The goal of the present study was to investigate the ovarian reserve of patients with SLE by measuring anti-Müllerian hormone (AMH) levels, and compare it to that of healthy controls.
Method
This was a case-control study performed on 80 premenopausal women, of whom 40 fulfilled the 1997 American College of Rheumatology (ACR) criteria for SLE and 40 healthy controls paired by oral contraceptive use. Serum concentrations of AMH in peripheral venous blood were measured using a human AMH ELISA kit (CUSABIO, Wuhan, China).
Results
AMH serum levels did not differ between patients with SLE and controls (22.79 ± 17.32 ng/ml versus 21.41 ± 16.22 ng/ml, respectively, p = 0.7), even after adjusting for age (21.03 ± 2.074 ng/ml versus 23.97 ± 2.71 ng/ml; p = 0.5). AHM levels were not significantly correlated with disease duration (r = 0.2; p = 0.3), body mass index (r = 0.2; p = 0.2) and disease activity (SLEDAI (r = 0.1; p = 0.7)) and damage indices (SLICC (r = 0.1; p = 0.7)). No associations were found between AMH and ethnicity, current smoking, as well as current or prior use of cyclophosphamide and other immunosuppressants.
Conclusion
In this cross-sectional study, women with SLE demonstrated similar AMH levels as healthy controls, suggesting preserved ovarian reserve in this population.
SwaakAJHuysenVNossentJCSmeenkRJ. Antinuclear antibody profiles in relation to specific disease manifestations of systemic lupus erythematosus. Clin Rheumatol1990; 9(1 Suppl 1): 82–94.
2.
GayedMGordonC. Pregnancy and rheumatic diseases. Rheumatology (Oxford)2007; 46: 1634–1640.
3.
AppenzellerSBlatytaPFCostallatLT. Ovarian failure in SLE patients using pulse cyclophosphamide: Comparison of different regimes. Rheumatol Int2008; 28: 567–571.
4.
UlugPOnerGKasapBAkbasEMOzcicekF. Evaluation of ovarian reserve tests in women with systemic lupus erythematosus. Am J Reprod Immunol2014; 72: 85–88.
5.
CarpHJASelmiCShoenfeldY. The autoimmune bases of infertility and pregnancy loss. J Autoimmun2012; 38: J266–J274.
6.
MangerKWildtLKaldenJRMangerB. Prevention of gonadal toxicity and preservation of gonadal function and fertility in young women with systemic lupus erythematosus treated by cyclophosphamide: The PREGO study. Autoimmun Rev2006; 5: 269–272.
7.
de AraujoDYamakamiLAikawaN. Ovarian reserve in adult patients with childhood-onset lupus: A possible deleterious effect of methotrexate?Scand J Rheumatol2014; 43: 503–511.
8.
BrouwerJHazesJMLavenJSDolhainRJ. Fertility in women with rheumatoid arthritis: influence of disease activity and medication. Ann Rheum Dis. Epub ahead of print 2014 May 15. DOI: 10.1136/annrheumdis-2014-205383.
9.
PfeiferSGoldbergJMcClureRD. Testing and interpreting measures of ovarian reserve: A committee opinion. Fertil Steril2012; 98: 1407–1415.
10.
La MarcaASpadaEGrisendiV. Normal serum anti-Müllerian hormone levels in the general female population and the relationship with reproductive history. Eur J Obstet Gynecol Reprod Biol2012; 163: 180–184.
11.
HehenkampWJLoomanCWThemmenAPde JongFHTe VeldeERBroekmansFJ. Anti-Müllerian hormone levels in the spontaneous menstrual cycle do not show substantial fluctuation. J Clin Endocrinol Metab2006; 91: 4057–4063.
12.
LawrenzBHenesJCHenesM. Impact of systemic lupus erythematosus on ovarian reserve in premenopausal women: Evaluation by using anti-Muellerian hormone. Lupus2011; 20: 1193–1197.
13.
MokCCChanPTToCH. Anti-Müllerian hormone and ovarian reserve in systemic lupus erythematosus. Arthritis Rheum2013; 65: 206–210.
14.
MorelNBachelotAGhillani-DalbinPAmouraZGalicierL. Study of anti-Müllerian hormone and the relationship with subsequent probability of pregnancy in 112 systemic lupus erythematosus patients exposed or not to cyclophosphamide. Lupus2013; 22: 16–16.
15.
MalheiroOBRezendeCPFerreiraGAReisFM. Ovarian reserve markers in reproductive age women with systemic lupus erythematosus. Lupus2013; 22: 162–162.
16.
MaWZhanZLiangXChenJHuangXLiaoC. Subclinical impairment of ovarian reserve in systemic lupus erythematosus patients with normal menstruation not using alkylating therapy. J Womens Health (Larchmt)2013; 22: 1023–1027.
17.
Velarde-OchoaMDEsquivel-ValerioJAVega-MoralesDSkinner-TaylorCMGalarza-DelgadoDAGarza-ElizondoMA. Anti-Müllerian hormone in reproductive age women with systemic lupus erythematosus [article in English, Spanish]. Reumatol Clin2014; 11: 78–82.
18.
ChenDYuanSZhanZZhanYYangXLiangL. Assessment of ovarian reserve with anti-Müllerian hormone in female patients with systemic lupus erythematosus. Zhonghua Yi Xue Za Zhi2014; 94: 977–980.
19.
TanEMCohenASFriesJF. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum1982; 25: 1271–1277.
20.
HochbergMC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum1997; 40: 1725–1725.
21.
VitaliCBombardieriSJonssonR. European Study Group on Classification Criteria for Sjögren’s Syndrome. Classification criteria for Sjögren’s syndrome: A revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis2002; 61: 554–558.
22.
NarkwicheanAJayaprakasanKMaaloufWEHernandez-MedranoJHPincott-AllenCCampbellBK. Effects of dehydroepiandrosterone on in vivo ovine follicular development. Hum Reprod2014; 29: 146–154.
23.
BombardierCGladmanDDUrowitzMBCaronDChangCH. Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum1992; 35: 630–640.
24.
GladmanDGinzlerEGoldsmithC. The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum1996; 39: 363–369.
BleilMEGregorichSEAdlerNESternfeldBRosenMPCedarsMI. Race/ethnic disparities in reproductive age: An examination of ovarian reserve estimates across four race/ethnic groups of healthy, regularly cycling women. Fertil Steril2014; 101: 199–207.
27.
Schuh-HuertaSMJohnsonNARosenMPSternfeldBCedarsMIReijo PeraRA. Genetic markers of ovarian follicle number and menopause in women of multiple ethnicities. Hum Genet2012; 131: 1709–1724.
28.
Saloum de Neves MantaFPereiraRViannaR. Revisiting the genetic ancestry of Brazilians using autosomal AIM-Indels. PloS One2013; 8: e75145–e75145.
29.
FreemanEWGraciaCRSammelMDLinHLimLCStraussJF3rd. Association of anti-Mullerian hormone levels with obesity in late reproductive-age women. Fertil Steril2007; 87: 101–106.
30.
SteinerAZStanczykFZPatelSEdelmanA. Antimullerian hormone and obesity: Insights in oral contraceptive users. Contraception2010; 81: 245–248.
31.
HalawatySElKattanEAzabHElGhamryNAl-InanyH. Effect of obesity on parameters of ovarian reserve in premenopausal women. J Obstet Gynaecol Can2010; 32: 687–690.
32.
OverbeekABroekmansFJHehenkampWJ. Intra-cycle fluctuations of anti-Mullerian hormone in normal women with a regular cycle: A re-analysis. Reprod Biomed Online2012; 24: 664–669.
33.
La MarcaAPapaleoEGrisendiVArgentoCGiuliniSVolpeA. Development of a nomogram based on markers of ovarian reserve for the individualisation of the follicle-stimulating hormone starting dose in in vitro fertilization cycles. BJOG2012; 119: 1171–1179.
34.
PlanteBJCooperGSBairdDDSteinerAZ. The impact of smoking on antimullerian hormone levels in women aged 38 to 50 years. Menopause2010; 17: 571–576.
35.
FréourTMassonDDessolleL. Ovarian reserve and in vitro fertilization cycles outcome according to women smoking status and stimulation regimen. Arch Gynecol Obstet2012; 285: 1177–1182.
36.
NardoLGChristodoulouDGouldDRobertsSAFitzgeraldCTLaingI. Anti-Müllerian hormone levels and antral follicle count in women enrolled in in vitro fertilization cycles: Relationship to lifestyle factors, chronological age and reproductive history. Gynecol Endocrinol2007; 23: 486–493.
37.
DafopoulosADafopoulosKGeorgouliasP. Smoking and AMH levels in women with normal reproductive history. Arch Gynecol Obstet2010; 282: 215–219.
38.
WaylenALJonesGLLedgerWL. Effect of cigarette smoking upon reproductive hormones in women of reproductive age: A retrospective analysis. Reprod Biomed Online2010; 20: 861–865.
39.
BartelsEMRibel-MadsenS. Cytokine measurements and possible interference from heterophilic antibodies—problems and solutions experienced with rheumatoid factor. Methods2013; 61: 18–22.
