2020 American College of Rheumatology Guideline for the Management of Reproductive Health in Rheumatic and Musculoskeletal Diseases

Lisa R Sammaritano, Bonnie L Bermas, Eliza E Chakravarty, Christina Chambers, Megan E B Clowse, Michael D Lockshin, Wendy Marder, Gordon Guyatt, D Ware Branch, Jill Buyon, Lisa Christopher-Stine, Rachelle Crow-Hercher, John Cush, Maurice Druzin, Arthur Kavanaugh, Carl A Laskin, Lauren Plante, Jane Salmon, Julia Simard, Emily C Somers, Virginia Steen, Sara K Tedeschi, Evelyne Vinet, C Whitney White, Jinoos Yazdany, Medha Barbhaiya, Brittany Bettendorf, Amanda Eudy, Arundathi Jayatilleke, Amit Aakash Shah, Nancy Sullivan, Laura L Tarter, Mehret Birru Talabi, Marat Turgunbaev, Amy Turner, Kristen E D'Anci, Lisa R Sammaritano, Bonnie L Bermas, Eliza E Chakravarty, Christina Chambers, Megan E B Clowse, Michael D Lockshin, Wendy Marder, Gordon Guyatt, D Ware Branch, Jill Buyon, Lisa Christopher-Stine, Rachelle Crow-Hercher, John Cush, Maurice Druzin, Arthur Kavanaugh, Carl A Laskin, Lauren Plante, Jane Salmon, Julia Simard, Emily C Somers, Virginia Steen, Sara K Tedeschi, Evelyne Vinet, C Whitney White, Jinoos Yazdany, Medha Barbhaiya, Brittany Bettendorf, Amanda Eudy, Arundathi Jayatilleke, Amit Aakash Shah, Nancy Sullivan, Laura L Tarter, Mehret Birru Talabi, Marat Turgunbaev, Amy Turner, Kristen E D'Anci

Abstract

Objective: To develop an evidence-based guideline on contraception, assisted reproductive technologies (ART), fertility preservation with gonadotoxic therapy, use of menopausal hormone replacement therapy (HRT), pregnancy assessment and management, and medication use in patients with rheumatic and musculoskeletal disease (RMD).

Methods: We conducted a systematic review of evidence relating to contraception, ART, fertility preservation, HRT, pregnancy and lactation, and medication use in RMD populations, using Grading of Recommendations Assessment, Development and Evaluation methodology to rate the quality of evidence and a group consensus process to determine final recommendations and grade their strength (conditional or strong). Good practice statements were agreed upon when indirect evidence was sufficiently compelling that a formal vote was unnecessary.

Results: This American College of Rheumatology guideline provides 12 ungraded good practice statements and 131 graded recommendations for reproductive health care in RMD patients. These recommendations are intended to guide care for all patients with RMD, except where indicated as being specific for patients with systemic lupus erythematosus, those positive for antiphospholipid antibody, and/or those positive for anti-Ro/SSA and/or anti-La/SSB antibodies. Recommendations and good practice statements support several guiding principles: use of safe and effective contraception to prevent unplanned pregnancy, pre-pregnancy counseling to encourage conception during periods of disease quiescence and while receiving pregnancy-compatible medications, and ongoing physician-patient discussion with obstetrics/gynecology collaboration for all reproductive health issues, given the overall low level of available evidence that relates specifically to RMD.

Conclusion: This guideline provides evidence-based recommendations developed and reviewed by panels of experts and RMD patients. Many recommendations are conditional, reflecting a lack of data or low-level data. We intend that this guideline be used to inform a shared decision-making process between patients and their physicians on issues related to reproductive health that incorporates patients' values, preferences, and comorbidities.

© 2019, American College of Rheumatology.

References

    1. Smyth A, Oliveira GH, Lahr BD, Bailey KR, Norby SM, Garovic VD. A systematic review and meta-analysis of pregnancy outcomes in patients with systemic lupus erythematosus and lupus nephritis. Clin J Am Soc Nephrol 2010;5:2060-8.
    1. Smith CJ, Förger F, Bandoli G, Chambers CD. Factors associated with preterm delivery among women with rheumatoid arthritis and women with juvenile idiopathic arthritis. Arthritis Care Res (Hoboken) 2019;71:1019-27.
    1. Langen ES, Chakravarty EF, Liaquat M, El-Sayed YY, Druzin ML. High rate of preterm birth in pregnancies complicated by rheumatoid arthritis. Am J Perinatol 2014;31:9-13.
    1. Chakravarty EF, Nelson L, Krishnan E. Obstetric hospitalizations in the United States for women with systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 2006;54:899-907.
    1. Bharti B, Lee SJ, Lindsay SP, Wingard DL, Jones KL, Lemus H, et al. Disease severity and pregnancy outcomes in women with rheumatoid arthritis: results from the Organization of Teratology Information Specialists Autoimmune Diseases in Pregnancy Project. J Rheumatol 2015;42:1376-82.
    1. Borella E, Lojacono A, Gatto M, Andreoli L, Taglietti M, Iaccarino L, et al. Predictors of maternal and fetal complications in SLE patients: a prospective study. Immunol Res 2014;60:170-6.
    1. Ruiz-Irastorza G, Lima F, Alves J, Khamashta MA, Simpson J, Hughes GR, et al. Increased rate of lupus flare during pregnancy and the puerperium: a prospective study of 78 pregnancies. Br J Rheumatol 1996;35:133-8.
    1. Barrett JH, Brennan P, Fiddler M, Silman AJ. Does rheumatoid arthritis remit during pregnancy and relapse postpartum? Results from a nationwide study in the United Kingdom performed prospectively from late pregnancy. Arthritis Rheum 1999;42:1219-27.
    1. Section on Breastfeeding. Breastfeeding and the use of human milk. Pediatrics 2012;129:e827-41.
    1. Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 2006;4:295-306.
    1. Schwarz EB, Manzi S. Risk of unintended pregnancy among women with systemic lupus erythematosus. Arthritis Rheum 2008;59:863-6.
    1. Yazdany J, Trupin L, Kaiser R, Schmajuk G, Gillis JZ, Chakravarty E, et al. Contraceptive counseling and use among women with systemic lupus erythematosus: a gap in health care quality? Arthritis Care Res (Hoboken) 2011;63:358-65.
    1. Østensen M, von Esebeck M, Villiger PM. Therapy with immunosuppressive drugs and biological agents and use of contraception in patients with rheumatic disease. J Rheumatol 2007;34:1266-9.
    1. Allen D, Hunter MS, Wood S, Beeson T. One Key Question®: first things first in reproductive health. Matern Child Health J 2017;21:387-92.
    1. Amy JJ, Tripathi V. Contraception for women: an evidence based overview. BMJ 2009;339:b2895.
    1. Winner B, Peipert JF, Zhao Q, Buckel C, Madden T, Allsworth JE, et al. Effectiveness of long-acting reversible contraception. N Engl J Med 2012;366:1998-2007.
    1. Committee on Gynecologic Practice Long-Acting Reversible Contraception Working Group. Committee opinion no. 642: increasing access to contraceptive implants and intrauterine devices to reduce unintended pregnancy. Obstet Gynecol 2015;126:e44-8.
    1. Curtis KM, Tepper NK, Jatlaoui TC, Berry-Bibee E, Horton LG, Zapata LB, et al. U.S. medical eligibility criteria for contraceptive use, 2016. MMWR Recomm Rep 2016;65:1-103.
    1. Petri M, Kim MY, Kalunian KC, Grossman J, Hahn BH, Sammaritano LR, et al. Combined oral contraceptives in women with systemic lupus erythematosus. N Engl J Med 2005;353:2550-8.
    1. Sánchez-Guerrero J, Uribe AG, Jiménez-Santana L, Mestanza-Peralta M, Lara-Reyes P, Seuc AH, et al. A trial of contraceptive methods in women with systemic lupus erythematosus. N Engl J Med 2005;353:2539-49.
    1. Julkunen HA, Kaaja R, Friman C. Contraceptive practice in women with systemic lupus erythematosus. Br J Rheumatol 1993;32:227-30.
    1. Galzote RM, Rafie S, Teal R, Mody SK. Transdermal delivery of combined hormonal contraception: a review of the current literature. Int J Womens Health 2017;9:315-21.
    1. Van den Heuvel MW, van Bragt AJ, Alnabawy AK, Kaptein MC. Comparison of ethinylestradiol pharmacokinetics in three hormonal contraceptive formulations: the vaginal ring, the transdermal patch and an oral contraceptive. Contraception 2005;72:168-74.
    1. Stam-Slob MC, Lambalk CB, van de Ree MA. Contraceptive and hormonal treatment options for women with history of venous thromboembolism. BMJ 2015;351:h4847.
    1. ACOG Committee on Practice Bulletins-Gynecology. ACOG practice bulletin no. 73: use of hormonal contraception in women with coexisting medical conditions. Obstet Gynecol 2006;107:1453-72.
    1. World Health Organization Department of Reproductive Health. Medical eligibility criteria for contraceptive use. 5th ed. 2015.
    1. Mantha S, Karp R, Raghavan V, Terrin N, Bauer KA, Zwicker JI. Assessing the risk of venous thromboembolic events in women taking progestin-only contraception: a meta-analysis. BMJ 2012;345:e4944.
    1. Conard J, Plu-Bureau G, Bahi N, Horellou MH, Pelissier C, Thalabard JC. Progestogen-only contraception in women at high risk of venous thromboembolism. Contraception 2004;70:437-41.
    1. Le Moigne E, Tromeur C, Delluc A, Gouillou M, Alavi Z, Lacut K, et al. Risk of recurrent venous thromboembolism on progestin-only contraception: a cohort study. Haematologica 2016;101:e12-4.
    1. Pisoni CN, Cuadrado MJ, Khamashta MA, Hunt BJ. Treatment of menorrhagia associated with oral anticoagulation: efficacy and safety of the levonorgestrel releasing intrauterine device (Mirena coil). Lupus 2006;15:877-80.
    1. Van Vlijmen EF, Veeger NJ, Middeldorp S, Hamulyák K, Prins MH, Büller HR, et al. Thrombotic risk during oral contraceptive use and pregnancy in women with factor V Leiden or prothrombin mutation: a rational approach to contraception. Blood 2011;118:2055-61.
    1. Stringer EM, Kaseba C, Levy J, Sinkala M, Goldenberg RL, Chi BH, et al. A randomized trial of the intrauterine contraceptive device vs hormonal contraception in women who are infected with the human immunodeficiency virus. Am J Obstet Gynecol 2007;197:144.e1-8.
    1. Krajewski CM, Geetha D, Gomez-Lobo V. Contraceptive options for women with a history of solid-organ transplantation. Transplantation 2013;95:1183-6.
    1. Huguelet PS, Sheehan C, Spitzer RF, Scott S. Use of the levonorgestrel 52-mg intrauterine system in adolescent and young adult solid organ transplant recipients: a case series. Contraception 2017;95:378-81.
    1. Clark M, Sowers M, Levy B, Nichols S. Bone mineral density loss and recovery during 48 months in first-time users of depot medroxyprogesterone acetate. Fertil Steril 2006;86:1466-74.
    1. Welcome to the mycophenolate REMS (Risk Evaluation and Mitigation Strategy). URL: https​://www.mycop​henol​atere​.
    1. Cellcept (mycophenolate mofetil) prescribing information. San Francisco (CA): 2019. Genentech; 2019. URL: .
    1. Mycophenolate: updated recommendations for contraception for men and women. December 2017. URL: https​://.
    1. Bellver J, Pellicer A. Ovarian stimulation for ovulation induction and in vitro fertilization in patients with systemic lupus erythematosus and antiphospholipid syndrome. Fertil Steril 2009;92:1803-10.
    1. Huong DL, Wechsler B, Vauthier-Brouzes D, Duhaut P, Costedoat N, Lefebvre G, et al. Importance of planning ovulation induction therapy in systemic lupus erythematosus and antiphospholipid syndrome: a single center retrospective study of 21 cases and 114 cycles. Semin Arthritis Rheum 2002;32:174-88.
    1. Orquevaux P, Masseau A, Le Guern V, Gayet V, Vauthier D, Guettrot-Imbert G, et al. In vitro fertilization in 37 women with systemic lupus erythematosus or antiphospholipid syndrome: a series of 97 procedures. J Rheumatol 2017;44:613-8.
    1. Guballa N, Sammaritano L, Schwartzman S, Buyon J, Lockshin MD. Ovulation induction and in vitro fertilization in systemic lupus erythematosus and antiphospholipid syndrome. Arthritis Rheum 2000;43:550-6.
    1. Chan WS, Dixon ME. The “ART” of thromboembolism: a review of assisted reproductive technology and thromboembolic complications. Thromb Res 2008;121:713-26.
    1. Nelson SM, Greer IA. Artificial reproductive technology and the risk of venous thromboembolic disease. J Thromb Haemost 2006;4:1661-3.
    1. Chan WS. The ‘ART’ of thrombosis: a review of arterial and venous thrombosis in assisted reproductive technology. Curr Opin Obstet Gynecol 2009;21:207-18.
    1. Yinon Y, Pauzner R, Dulitzky M, Elizur SE, Dor J, Shulman A. Safety of IVF under anticoagulant therapy in patients at risk for thrombo-embolic events. Reprod Biomed Online 2006;12:354-8.
    1. Nelson SM. Venous thrombosis during assisted reproduction: novel risk reduction strategies. Thromb Res 2013;131 Suppl 1:S1-3.
    1. Mok CC, Lau CS, Wong RW. Risk factors for ovarian failure in patients with systemic lupus erythematosus receiving cyclophosphamide therapy. Arthritis Rheum 1998;41:831-7.
    1. Tamirou F, Husson SN, Gruson D, Debiève F, Lauwerys BR, Houssiau FA. The Euro-Lupus low-dose intravenous cyclophosphamide regimen does not impact the ovarian reserve, as measured by serum levels of anti-Müllerian hormone. Arthritis Rheumatol 2017;69:1267-71.
    1. Oktay K, Harvey BE, Partridge AH, Quinn GP, Reinecke J, Taylor HS, et al. Fertility preservation in patients with cancer: ASCO clinical practice guideline update. J Clin Oncol 2018;36:1994-2001.
    1. Moore HC, Unger JM, Phillips KA, Boyle F, Hitre E, Porter D, et al. Goserelin for ovarian protection during breast-cancer adjuvant chemotherapy. N Engl J Med 2015;372:923-32.
    1. Blumenfeld Z, Mischari O, Schultz N, Boulman N, Balbir-Gurman A. Gonadotropin releasing hormone agonists may minimize cyclophosphamide associated gonadotoxicity in SLE and autoimmune diseases. Semin Arthritis Rheum 2011;41:346-52.
    1. Brunner HI, Silva CA, Reiff A, Higgins GC, Imundo L, Williams CB, et al. Randomized, double-blind, dose-escalation trial of triptorelin for ovary protection in childhood-onset systemic lupus erythematosus. Arthritis Rheumatol 2015;67:1377-85.
    1. Koga T, Umeda M, Endo Y, Ishida M, Fujita Y, Tsuji S, et al. Effect of a gonadotropin-releasing hormone analog for ovarian function preservation after intravenous cyclophosphamide therapy in systemic lupus erythematosus patients: a retrospective inception cohort study. Int J Rheum Dis 2018;21:1287-92.
    1. Pagnoux C, Le Guern V, Goffinet F, Diot E, Limal N, Pannier E, et al. Pregnancies in systemic necrotizing vasculitides: report on 12 women and their 20 pregnancies. Rheumatology (Oxford) 2011;50:953-61.
    1. Somers EC, Marder W, Christman GM, Ognenovski V, McCune WJ. Use of a gonadotropin-releasing hormone analog for protection against premature ovarian failure during cyclophosphamide therapy in women with severe lupus. Arthritis Rheum 2005;52:2761-7.
    1. Soares PM, Borba EF, Bonfa E, Hallak J, Corrêa AL, Silva CA. Gonad evaluation in male systemic lupus erythematosus. Arthritis Rheum 2007;56:2352-61.
    1. Wyrobek AJ, Schmid TE, Marchetti F. Relative susceptibilities of male germ cells to genetic defects induced by cancer chemotherapies. J Natl Cancer Inst Monogr 2005;2005:31-5.
    1. Stahl PJ, Stember DS, Hsiao W, Schlegel PN. Indications and strategies for fertility preservation in men. Clin Obstet Gynecol 2010;53:815-27.
    1. ACOG Practice Bulletin no. 141: management of menopausal symptoms. Obstet Gynecol 2014;123:202-16.
    1. The NAMS 2017 Hormone Therapy Position Statement Advisory Panel. The 2017 hormone therapy position statement of the North American Menopause Society. Menopause 2017;24:728-53.
    1. U.S. Preventive Services Task Force. Hormone therapy for the prevention of chronic conditions in postmenopausal women: recommendations from the U.S. Preventive Services Task Force. Ann Intern Med 2005;142:855-60.
    1. Beral V, Million Women Study Collaborators. Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 2003;362:419-27.
    1. North American Menopause Society. The 2012 hormone therapy position statement of the North American Menopause Society. Menopause 2012;19:257-71.
    1. Buyon JP, Petri MA, Kim MY, Kalunian KC, Grossman J, Hahn BH, et al. The effect of combined estrogen and progesterone hormone replacement therapy on disease activity in systemic lupus erythematosus: a randomized trial. Ann Intern Med 2005;142:953-62.
    1. Mok CC, Lau CS, Ho CT, Lee KW, Mok MY, Wong RW. Safety of hormonal replacement therapy in postmenopausal patients with systemic lupus erythematosus. Scand J Rheumatol 1998;27:342-6.
    1. Sánchez-Guerrero J, González-Pérez M, Durand-Carbajal M, Lara-Reyes P, Jiménez-Santana L, Romero-Díaz J, et al. Menopause hormonal therapy in women with systemic lupus erythematosus. Arthritis Rheum 2007;56:3070-9.
    1. Kreidstein S, Urowitz MB, Gladman DD, Gough J. Hormone replacement therapy in systemic lupus erythematosus. J Rheumatol 1997;24:2149-52.
    1. Marjoribanks J, Farquhar C, Roberts H, Lethaby A, Lee J. Long-term hormone therapy for perimenopausal and postmenopausal women. Cochrane Database Syst Rev 2017;1:CD004143.
    1. Cushman M, Kuller LH, Prentice R, Rodabough RJ, Psaty BM, Stafford RS, et al. Estrogen plus progestin and risk of venous thrombosis. JAMA 2004;292:1573-80.
    1. Canonico M, Oger E, Plu-Bureau G, Conard J, Meyer G, Lévesque H, et al, for the Estrogen and Thromboembolism Risk (ESTHER) Study Group. Hormone therapy and venous thromboembolism among postmenopausal women-impact of the route of estrogen administration and progestogens: the ESTHER study. Circulation 2007;20;115:840-5.
    1. Sweetland S, Beral V, Balkwill A, Liu B, Benson VS, Canonico M, et al. Venous thromboembolism risk in relation to use of different types of postmenopausal hormone therapy in a large prospective study. J Thromb Haemost 2012;10:2277-86.
    1. Smith NL, Heckbert SR, Lemaitre RN, Reiner AP, Lumley T, Weiss NS, et al. Esterified estrogens and conjugated equine estrogens and the risk of venous thrombosis. JAMA 2004;292:1581-7.
    1. Rovinski D, Ramos RB, Fighera TM, Casanova GK, Spritzer PM. Risk of venous thromboembolism events in postmenopausal women using oral versus non-oral hormone therapy: a systematic review and meta-analysis. Thromb Res 2018;168:83-95.
    1. Straczek C, Oger E, Yon de Jonage-Canonico MB, Plu-Bureau G, Conard J, Meyer G, et al, for the Estrogen and Thromboembolism Risk (ESTHER) Study Group. Prothrombotic mutations, hormone therapy, and venous thromboembolism among postmenopausal women: impact of the route of estrogen administration. Circulation 2005;112:3495-500.
    1. Rosendaal FR, Vessey M, Rumley A, Daly E, Woodward M, Helmerhorst FM, et al. Hormonal replacement therapy, prothrombotic mutations and the risk of venous thrombosis. Br J Haematol 2002;116:851-4.
    1. Canonico M, Plu-Bureau G, Lowe GD, Scarabin PY. Hormone replacement therapy and risk of venous thromboembolism in postmenopausal women: systematic review and meta-analysis. BMJ 2008;336:1227-31.
    1. Cravioto MD, Durand-Carbajal M, Jiménez-Santana L, Lara-Reyes P, Seuc AH, Sánchez-Guerrero J. Efficacy of estrogen plus progestin on menopausal symptoms in women with systemic lupus erythematosus: a randomized, double-blind, controlled trial. Arthritis Care Res (Hoboken) 2011;63:1654-63.
    1. Gupta R, Deepanjali S, Kumar A, Dadhwal V, Agarwal SK, Pandey RM, et al. A comparative study of pregnancy outcomes and menstrual irregularities in northern Indian patients with systemic lupus erythematosus and rheumatoid arthritis. Rheumatol Int 2010;30:1581-5.
    1. Lockshin MD. Pregnancy does not cause systemic lupus erythematosus to worsen. Arthritis Rheum 1989;32:665-70.
    1. Le Thi Huong D, Wechsler B, Piette JC, Bletry O, Godeau P. Pregnancy and its outcome in systemic lupus erythematosus. QJM 1994;87:721-9.
    1. Hussein Aly EA, Mohamed Riyad R, Nabil Mokbel A. Pregnancy outcome in patients with systemic lupus erythematosus: a single center study in the High Risk Pregnancy unit. Middle East Fertil Soc J 2016;21:168-74.
    1. Mintz G, Niz J, Gutierrez G, Garcia-Alonso A, Karchmer S. Prospective study of pregnancy in systemic lupus erythematosus: results of a multidisciplinary approach. J Rheumatol 1986;13:732-9.
    1. Mokbel A, Geilan AM, AboElgheit S. Could women with systemic lupus erythematosus (SLE) have successful pregnancy outcomes? Prospective observational study. Egypt Rheumatologist 2013;35:133-9.
    1. Mankee A, Petri M, Magder LS. Lupus anticoagulant, disease activity and low complement in the first trimester are predictive of pregnancy loss. Lupus Sci Med 2015;2:e000095.
    1. Tuin J, Sanders JS, de Joode AA, Stegeman CA. Pregnancy in women diagnosed with antineutrophil cytoplasmic antibody-associated vasculitis: outcome for the mother and the child. Arthritis Care Res (Hoboken) 2012;64:539-45.
    1. Whitelaw DA, Hall D, Kotze T. Pregnancy in systemic lupus erythematosus: a retrospective study from a developing community. Clin Rheumatol 2008;27:577-80.
    1. Croft AP, Smith SW, Carr S, Youssouf S, Salama AD, Burns A, et al. Successful outcome of pregnancy in patients with anti-neutrophil cytoplasm antibody-associated small vessel vasculitis. Kidney Int 2015;87:807-11.
    1. Tozman EC, Urowitz MB, Gladman DD. Systemic lupus erythematosus and pregnancy. J Rheumatol 1980;7:624-32.
    1. Ku M, Guo S, Shang W, Li Q, Zeng R, Han M, et al. Pregnancy outcomes in Chinese patients with systemic lupus erythematosus (SLE): a retrospective study of 109 pregnancies. PLoS One 2016;11:e0159364.
    1. Kothari R, Digole A, Kamat S, Nandanwar YS, Gokhale Y. Reproductive health in systemic lupus erythematosus, an experience from government hospital in western India. J Assoc Physicians India 2016;64:16-20.
    1. Skorpen CG, Lydersen S, Gilboe IM, Skomsvoll JF, Salvesen KÅ, Palm Ø, et al. Influence of disease activity and medications on offspring birth weight, pre-eclampsia and preterm birth in systemic lupus erythematosus: a population-based study. Ann Rheum Dis 2018;77:264-9.
    1. Phansenee S, Sekararithi R, Jatavan P, Tongsong T. Pregnancy outcomes among women with systemic lupus erythematosus: a retrospective cohort study from Thailand. Lupus 2018;27:158-64.
    1. Rahman FZ, Rahman J, Al-Suleiman SA, Rahman MS. Pregnancy outcome in lupus nephropathy. Arch Gynecol Obstet 2005;271:222-6.
    1. Bobrie G, Liote F, Houillier P, Grünfeld JP, Jungers P. Pregnancy in lupus nephritis and related disorders. Am J Kidney Dis 1987;9:339-43.
    1. Jungers P, Dougados M, Pélissier C, Kuttenn F, Tron F, Lesavre P, et al. Lupus nephropathy and pregnancy: report of 104 cases in 36 patients. Arch Intern Med 1982;142:771-6.
    1. Gaballa HA, El-Shahawy EE, Atta DS, Gerbash EF. Clinical and serological risk factors of systemic lupus erythematosus outcomes during pregnancy. Egypt Rheumatologist 2012;34:159-65.
    1. Tedeschi SK, Massarotti E, Guan H, Fine A, Bermas BL, Costenbader KH. Specific systemic lupus erythematosus disease manifestations in the six months prior to conception are associated with similar disease manifestations during pregnancy. Lupus 2015;24:1283-92.
    1. Palmsten K, Rolland M, Hebert MF, Clowse ME, Schatz M, Xu R, et al. Patterns of prednisone use during pregnancy in women with rheumatoid arthritis: daily and cumulative dose. Pharmacoepidemiol Drug Saf 2018;27:430-8.
    1. Zanatta E, Polito P, Favaro M, Larosa M, Marson P, Cozzi F, et al. Therapy of scleroderma renal crisis: state of the art. Autoimmun Rev 2018;17:882-9.
    1. Bullo M, Tschumi S, Bucher BS, Bianchetti MG, Simonetti GD. Pregnancy outcome following exposure to angiotensin-converting enzyme inhibitors or angiotensin receptor antagonists: a systematic review. Hypertension 2012;60:444-50.
    1. Liu EL, Liu Z, Zhou YX. Feasibility of hydroxychloroquine adjuvant therapy in pregnant women with systemic lupus erythematosus. Biomed Res 2018;29:980-3.
    1. Leroux M, Desveaux C, Parcevaux M, Julliac B, Gouyon JB, Dallay D, et al. Impact of hydroxychloroquine on preterm delivery and intrauterine growth restriction in pregnant women with systemic lupus erythematosus: a descriptive cohort study. Lupus 2015;24:1384-91.
    1. Eudy AM, Siega-Riz AM, Engel SM, Franceschini N, Howard AG, Clowse ME, et al. Effect of pregnancy on disease flares in patients with systemic lupus erythematosus. Ann Rheum Dis 2018;77:855-60.
    1. Clowse ME, Magder L, Witter F, Petri M. Hydroxychloroquine in lupus pregnancy. Arthritis Rheum 2006;54:3640-7.
    1. Diav-Citrin O, Blyakhman S, Shechtman S, Ornoy A. Pregnancy outcome following in utero exposure to hydroxychloroquine: a prospective comparative observational study. Reprod Toxicol 2013;39:58-62.
    1. Hwang JK, Park HK, Sung YK, Hoh JK, Lee HJ. Maternal outcomes and follow-up of preterm and term neonates born to mothers with systemic lupus erythematosus. J Matern Fetal Neonatal Med 2018;31:7-13.
    1. Kroese SJ, de Hair MJ, Limper M, Lely AT, van Laar JM, Derksen RH, et al. Hydroxychloroquine use in lupus patients during pregnancy is associated with longer pregnancy duration in preterm births. J Immunol Res 2017;2017:2810202.
    1. Georgiou PE, Politi EN, Katsimbri P, Sakka V, Drosos AA. Outcome of lupus pregnancy: a controlled study. Rheumatology (Oxford) 2000;39:1014-9.
    1. Teh CL, Wong JS, Ngeh NK, Loh WL. Systemic lupus erythematosus pregnancies: a case series from a tertiary, East Malaysian hospital. Lupus 2009;18:278-82.
    1. Ruffatti A, Tonello M, Hoxha A, Sciascia S, Cuadrado M, Latino JO, et al. Effect of additional treatments combined with conventional therapies in pregnant patients with high-risk antiphospholipid syndrome: a multicentre study. Thromb Haemost 2018;118:639-46.
    1. ACOG committee opinion no. 743: low-dose aspirin use during pregnancy. Obstet Gynecol 2018;132:e44-52.
    1. LeFevre ML, US Preventive Services Task Force. Low-dose aspirin use for the prevention of morbidity and mortality from preeclampsia: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 2014;161:819-26.
    1. Buyon JP, Kim MY, Guerra MM, Laskin CA, Petri M, Lockshin MD, et al. Predictors of pregnancy outcomes in patients with lupus: a cohort study. Ann Intern Med 2015;163:153-63.
    1. Abheiden CN, Blomjous BS, Kroese SJ, Bultink IE, Fritsch-Stork RD, Lely AT, et al. Low-molecular-weight heparin and aspirin use in relation to pregnancy outcome in women with systemic lupus erythematosus and antiphospholipid syndrome: a cohort study. Hypertens Pregnancy 2017;36:8-15.
    1. Moroni G, Doria A, Giglio E, Imbasciati E, Tani C, Zen M, et al. Maternal outcome in pregnant women with lupus nephritis: a prospective multicenter study. J Autoimmun 2016;74:194-200.
    1. Imbasciati E, Tincani A, Gregorini G, Doria A, Moroni G, Cabiddu G, et al. Pregnancy in women with pre-existing lupus nephritis: predictors of fetal and maternal outcome. Nephrol Dial Transplant 2009;24:519-25.
    1. Lockshin MD, Kim M, Laskin CA, Guerra M, Branch DW, Merrill J, et al. Prediction of adverse pregnancy outcome by the presence of lupus anticoagulant, but not anticardiolipin antibody, in patients with antiphospholipid antibodies. Arthritis Rheum 2012;64: 2311-8.
    1. Bao SH, Sheng SL, Liao H, Zhou Q, Frempong ST, Tu WY. Use of D-dimer measurement to guide anticoagulant treatment in recurrent pregnancy loss associated with antiphospholipid syndrome. Am J Reprod Immunol 2017;78:e12770.
    1. Farquharson RG, Quenby S, Greaves M. Antiphospholipid syndrome in pregnancy: a randomized, controlled trial of treatment. Obstet Gynecol 2002;100:408-13.
    1. Van Hoorn ME, Hague WM, van Pampus MG, Bezemer D, de Vries JI, for the FRUIT investigators. Low-molecular-weight heparin and aspirin in the prevention of recurrent early-onset pre-eclampsia in women with antiphospholipid antibodies: the FRUIT-RCT. Eur J Obstet Gynecol Reprod Biol 2016;197:168-73.
    1. Naru T, Khan RS, Ali R. Pregnancy outcome in women with antiphospholipid syndrome on low-dose aspirin and heparin: a retrospective study. East Mediterr Health J 2010;16:308-12.
    1. Goel N, Tuli A, Choudhry R. The role of aspirin versus aspirin and heparin in cases of recurrent abortions with raised anticardiolipin antibodies. Med Sci Monit 2006;12:CR132-6.
    1. Brewster JA, Shaw NJ, Farquharson RG. Neonatal and pediatric outcome of infants born to mothers with antiphospholipid syndrome. J Perinat Med 1999;27:183-7.
    1. Cohn DM, Goddijn M, Middeldorp S, Korevaar JC, Dawood F, Farquharson RG. Recurrent miscarriage and antiphospholipid antibodies: prognosis of subsequent pregnancy. J Thromb Haemost 2010;8:2208-13.
    1. Clark CA, Spitzer KA, Crowther MA, Nadler JN, Laskin MD, Waks JA, et al. Incidence of postpartum thrombosis and preterm delivery in women with antiphospholipid antibodies and recurrent pregnancy loss. J Rheumatol 2007;34:992-6.
    1. ACOG practice bulletin no. 196: thromboembolism in pregnancy. Obstet Gynecol 2018;132:e1-17.
    1. Brito-Zerón P, Izmirly PM, Ramos-Casals M, Buyon JP, Khamashta MA. The clinical spectrum of autoimmune congenital heart block. Nat Rev Rheumatol 2015;11:301-12.
    1. Wahren-Herlenius M, Sonesson SE, Clowse ME. Neonatal lupus erythematosus. In: Wallace D, Hahn B, editors. Dubois’ lupus erythematosus and related syndromes. 8th ed. Philadelphia: Saunders; 2012. p. 464-72.
    1. Izmirly PM, Rivera TL, Buyon JP. Neonatal lupus syndromes. Rheum Dis Clin North Am 2007;33:267-85.
    1. Kan N, Silverman ED, Kingdom J, Dutil N, Laskin C, Jaeggi E. Serial echocardiography for immune-mediated heart disease in the fetus: results of a risk-based prospective surveillance strategy. Prenat Diagn 2017;37:375-82.
    1. Izmirly PM, Costedoat-Chalumeau N, Pisoni CN, Khamashta MA, Kim MY, Saxena A, et al. Maternal use of hydroxychloroquine is associated with a reduced risk of recurrent anti-SSA/Ro-antibody-associated cardiac manifestations of neonatal lupus. Circulation 2012;126:76-82.
    1. Cuneo BF, Lee M, Roberson D, Niksch A, Ovadia M, Parilla BV, et al. A management strategy for fetal immune-mediated atrioventricular block. J Matern Fetal Neonatal Med 2010;23:1400-5.
    1. Friedman DM, Kim MY, Copel JA, Llanos C, Davis C, Buyon JP. Prospective evaluation of fetuses with autoimmune-associated congenital heart block followed in the PR Interval and Dexamethasone Evaluation (PRIDE) study. Am J Cardiol 2009;103:1102-6.
    1. Izmirly PM, Saxena A, Sahl SK, Shah U, Friedman DM, Kim MY, et al. Assessment of fluorinated steroids to avert progression and mortality in anti-SSA/Ro-associated cardiac injury limited to the fetal conduction system. Ann Rheum Dis 2016;75:1161-5.
    1. Colie CF. Male mediated teratogenesis. Reprod Toxicol 1993;7:3-9.
    1. Anderson D, Bishop JB, Garner RC, Ostrosky-Wegman P, Selby PB. Cyclophosphamide: review of its mutagenicity for an assessment of potential germ cell risks. Mutat Res 1995;330:115-81.
    1. Brandenburg NA, Bwire R, Freeman J, Houn F, Sheehan P, Zeldis JB. Effectiveness of risk evaluation and mitigation strategies (REMS) for lenalidomide and thalidomide: patient comprehension and knowledge retention. Drug Saf 2017;40:333-41.
    1. Teo SK, Harden JL, Burke AB, Noormohamed FH, Youle M, Johnson MA, et al. Thalidomide is distributed into human semen after oral dosing. Drug Metab Dispos 2001;29:1355-7.
    1. Larsen MD, Friedman S, Magnussen B, Nørgård BM. Birth outcomes in children fathered by men treated with anti-TNF-α agents before conception. Am J Gastroenterol 2016;111:1608-13.
    1. Nørgård BM, Magnussen B, Larsen MD, Friedman S. Reassuring results on birth outcomes in children fathered by men treated with azathioprine/6-mercaptopurine within 3 months before conception: a nationwide cohort study. Gut 2017;66:1761-6.
    1. Ben-Chetrit E, Berkun Y, Ben-Chetrit E, Ben-Chetrit A. The outcome of pregnancy in the wives of men with familial Mediterranean fever treated with colchicine. Semin Arthritis Rheum 2004;34:549-52.
    1. Weber-Schoendorfer C, Hoeltzenbein M, Wacker E, Meister R, Schaefer C. No evidence for an increased risk of adverse pregnancy outcome after paternal low-dose methotrexate: an observational cohort study. Rheumatology (Oxford) 2014;53:757-63.
    1. Eck LK, Jensen TB, Mastrogiannis D, Torp-Pedersen A, Askaa B, Nielsen TK, et al. Risk of adverse pregnancy outcome after paternal exposure to methotrexate within 90 days before pregnancy. Obstet Gynecol 2017;129:707-14.
    1. Winter RW, Larsen MD, Magnussen B, Friedman S, Kammerlander H, Nørgård BM. Birth outcomes after preconception paternal exposure to methotrexate: a nationwide cohort study. Reprod Toxicol 2017;74:219-23.
    1. Wallenius M, Lie E, Daltveit AK, Salvesen KÅ, Skomsvoll JF, Kalstad S, et al. No excess risks in offspring with paternal preconception exposure to disease-modifying antirheumatic drugs. Arthritis Rheumatol 2015;67:296-301.
    1. Kieseier BC, Benamor M. Pregnancy outcomes following maternal and paternal exposure to teriflunomide during treatment for relapsing-remitting multiple sclerosis. Neurol Ther 2014;3:133-8.
    1. Midtvedt K, Bergan S, Reisaeter AV, Vikse BE, Åsberg A. Exposure to mycophenolate and fatherhood. Transplantation 2017;101:e214-7.
    1. Jones A, Clary MJ, McDermott E, Coscia LA, Constantinescu S, Moritz MJ, et al. Outcomes of pregnancies fathered by solid-organ transplant recipients exposed to mycophenolic acid products. Prog Transplant 2013;23:153-7.
    1. Sands K, Jansen R, Zaslau S, Greenwald D. The safety of therapeutic drugs in male inflammatory bowel disease patients wishing to conceive [review]. Aliment Pharmacol Ther 2015;41:821-34.
    1. Youngstein T, Hoffmann P, Gül A, Lane T, Williams R, Rowczenio DM, et al. International multi-centre study of pregnancy outcomes with interleukin-1 inhibitors. Rheumatology (Oxford) 2017;56:2102-8.
    1. Ciron J, Audoin B, Bourre B, Brassat D, Durand-Dubief F, Laplaud D, et al. Recommendations for the use of rituximab in neuromyelitis optica spectrum disorders. Rev Neurol (Paris) 2018;174:255-64.
    1. Feldkamp M, Carey JC. Clinical teratology counseling and consultation case report: low dose methotrexate exposure in the early weeks of pregnancy. Teratology 1993;47:533-9.
    1. Kainz A, Harabacz I, Cowlrick IS, Gadgil SD, Hagiwara D. Review of the course and outcome of 100 pregnancies in 84 women treated with tacrolimus. Transplantation 2000;70:1718-21.
    1. Sifontis NM, Coscia LA, Constantinescu S, Lavelanet AF, Moritz MJ, Armenti VT. Pregnancy outcomes in solid organ transplant recipients with exposure to mycophenolate mofetil or sirolimus. Transplantation 2006;82:1698-702.
    1. Vargesson N. Thalidomide-induced teratogenesis: history and mechanisms. Birth Defects Res C Embryo Today 2015;105:140-56.
    1. Bérard A, Zhao JP, Shui I, Colilla S. Leflunomide use during pregnancy and the risk of adverse pregnancy outcomes. Ann Rheum Dis 2018;77:500-9.
    1. Weber-Schoendorfer C, Beck E, Tissen-Diabaté T, Schaefer C. Leflunomide-a human teratogen? A still not answered question: an evaluation of the German Embryotox pharmacovigilance database. Reprod Toxicol 2017;71:101-7.
    1. Connell W, Miller A. Treating inflammatory bowel disease during pregnancy: risks and safety of drug therapy. Drug Saf 1999;21:311-23.
    1. Indraratna PL, Virk S, Gurram D, Day RO. Use of colchicine in pregnancy: a systematic review and meta-analysis. Rheumatology (Oxford) 2018;57:382-7.
    1. Saavedra MÁ, Sánchez A, Morales S, Ángeles U, Jara LJ. Azathioprine during pregnancy in systemic lupus erythematosus patients is not associated with poor fetal outcome. Clin Rheumatol 2015;34:1211-6.
    1. Brouwer J, Hazes JM, Laven JS, Dolhain RJ. Fertility in women with rheumatoid arthritis: influence of disease activity and medication. Ann Rheum Dis 2015;74:1836-41.
    1. Koren G, Florescu A, Costei AM, Boskovic R, Moretti ME. Nonsteroidal antiinflammatory drugs during third trimester and the risk of premature closure of the ductus arteriosus: a meta-analysis. Ann Pharmacother 2006;40:824-9.
    1. Bröms G, Granath F, Ekbom A, Hellgren K, Pedersen L, Sørensen HT, et al. Low risk of birth defects for infants whose mothers are treated with anti-tumor necrosis factor agents during pregnancy. Clin Gastroenterol Hepatol 2016;14:234-41.
    1. Diav-Citrin O, Otcheretianski-Volodarsky A, Shechtman S, Ornoy A. Pregnancy outcome following gestational exposure to TNF-α-inhibitors: a prospective, comparative, observational study. Reprod Toxicol 2014;43:78-84.
    1. Mariette X, Förger F, Abraham B, Flynn AD, Moltó A, Flipo RM, et al. Lack of placental transfer of certolizumab pegol during pregnancy: results from CRIB, a prospective, postmarketing, pharmacokinetic study. Ann Rheum Dis 2018;77:228-33.
    1. Kane SV, Acquah LA. Placental transport of immunoglobulins: a clinical review for gastroenterologists who prescribe therapeutic monoclonal antibodies to women during conception and pregnancy. Am J Gastroenterol 2009;104:228-33.
    1. Chakravarty EF, Murray ER, Kelman A, Farmer P. Pregnancy outcomes after maternal exposure to rituximab. Blood 2011;117:1499-506.
    1. Sheard NF, Walker WA. The role of breast milk in the development of the gastrointestinal tract. Nutr Rev 1988;46:1-8.
    1. Hanson LA, Ahlstedt S, Andersson B, Carlsson B, Fällström SP, Mellander L, et al. Protective factors in milk and the development of the immune system. Pediatrics 1985;75:172-6.
    1. Ladomenou F, Moschandreas J, Kafatos A, Tselentis Y, Galanakis E. Protective effect of exclusive breastfeeding against infections during infancy: a prospective study. Arch Dis Child 2010;95:1004-8.
    1. Armstrong J, Reilly JJ. The prevalence of obesity and undernutrition in Scottish children: growth monitoring within the Child Health Surveillance Programme. Scott Med J 2003;48:32-7.
    1. Davis MK, Savitz DA, Graubard BI. Infant feeding and childhood cancer. Lancet 1988;2:365-8.
    1. Horta BL, Loret de Mola C, Victora CG. Long-term consequences of breastfeeding on cholesterol, obesity, systolic blood pressure and type 2 diabetes: a systematic review and meta-analysis [review]. Acta Paediatr 2015;104:30-7.
    1. Schwarz EB, Ray RM, Stuebe AM, Allison MA, Ness RB, Freiberg MS, et al. Duration of lactation and risk factors for maternal cardiovascular disease. Obstet Gynecol 2009;113:974-82.
    1. Newton ER, Hale TW. Drugs in breast milk. Clin Obstet Gynecol 2015;58:868-84.
    1. Motta M, Tincani A, Faden D, Zinzini E, Lojacono A, Marchesi A, et al. Follow-up of infants exposed to hydroxychloroquine given to mothers during pregnancy and lactation. J Perinatol 2005;25:86-9.
    1. Ben-Chetrit E, Scherrmann JM, Levy M. Colchicine in breast milk of patients with familial Mediterranean fever. Arthritis Rheum 1996;39:1213-7.
    1. Bragnes Y, Boshuizen R, de Vries A, Lexberg Å, Østensen M. Low level of rituximab in human breast milk in a patient treated during lactation [letter]. Rheumatology (Oxford) 2017;56:1047-8.
    1. Berlin CM Jr, Yaffe SJ. Disposition of salicylazosulfapyridine (Azulfidine) and metabolites in human breast milk. Dev Pharmacol Ther 1980;1:31-9.
    1. Fritzsche J, Pilch A, Mury D, Schaefer C, Weber-Schoendorfer C. Infliximab and adalimumab use during breastfeeding [letter]. J Clin Gastroenterol 2012;46:718-9.
    1. Gardiner SJ, Gearry RB, Roberts RL, Zhang M, Barclay ML, Begg EJ. Comment: breast-feeding during maternal use of azathioprine. Ann Pharmacother 2007;41:719-20.
    1. Bramham K, Chusney G, Lee J, Lightstone L, Nelson-Piercy C. Breastfeeding and tacrolimus: serial monitoring in breast-fed and bottle-fed infants. Clin J Am Soc Nephrol 2013;8:563-7.
    1. Matro R, Martin CF, Wolf D, Shah SA, Mahadevan U. Exposure concentrations of infants breastfed by women receiving biologic therapies for inflammatory bowel diseases and effects of breastfeeding on infections and development. Gastroenterology 2018;155:696-704.
    1. American Academy of Pediatrics Committee on Drugs. Transfer of drugs and other chemicals into human milk. Pediatrics 2001;108:776-89.
    1. Johns DG, Rutherford LD, Leighton PC, Vogel CL. Secretion of methotrexate into human milk. Am J Obstet Gynecol 1972;112:978-80.
    1. Andreoli L, Bertsias GK, Agmon-Levin N, Brown S, Cervera R, Costedoat-Chalumeau N, et al. EULAR recommendations for women's health and the management of family planning, assisted reproduction, pregnancy and menopause in patients with systemic lupus erythematosus and/or antiphospholipid syndrome. Ann Rheum Dis 2017;76:476-85.
    1. Flint J, Panchal S, Hurrell A, van de Venne M, Gayed M, Schreiber K, et al. BSR and BHPR guideline on prescribing drugs in pregnancy and breastfeeding-part I: Standard and biologic disease modifying anti-rheumatic drugs and corticosteroids. Rheumatology (Oxford) 2016;55:1693-7.
    1. Flint J, Panchal S, Hurrell A, van de Venne M, Gayed M, Schreiber K, et al. BSR and BHPR guideline on prescribing drugs in pregnancy and breastfeeding-part II: analgesics and other drugs used in rheumatology practice. Rheumatology (Oxford) 2016;55:1698-702.
    1. Götestam Skorpen C, Hoeltzenbein M, Tincani A, Fischer-Betz R, Elefant E, Chambers C, et al. The EULAR points to consider for use of antirheumatic drugs before pregnancy, and during pregnancy and lactation. Ann Rheum Dis 2016;75:795-810.
    1. Meng ML, Landau R, Viktorsdottir O, Banayan J, Grant T, Bateman B, et al. Pulmonary hypertension in pregnancy: a report of 49 cases at four tertiary North American sites. Obstet Gynecol 2017;129:511-20.
    1. Sangle SR, Vounotrypidis P, Briley A, Nel L, Lutalo PM, Sanchez-Fernandez S, et al. Pregnancy outcome in patients with systemic vasculitis: a single-centre matched case-control study. Rheumatology (Oxford) 2015;54:1582-6.
    1. Ritchie J, Smyth A, Tower C, Helbert M, Venning M, Garovic V. Maternal deaths in women with lupus nephritis: a review of published evidence. Lupus 2012;21:534-41.
    1. El-Sayed YY, Lu EJ, Genovese MC, Lambert RE, Chitkara U, Druzin ML. Central nervous system lupus and pregnancy: 11-year experience at a single center. J Matern Fetal Neonatal Med 2002;12:99-103.
    1. Society for Maternal-Fetal Medicine (SMFM). Executive summary: Reproductive Services for Women at High Risk for Maternal Mortality Workshop, February 11-12, 2019, Las Vegas, Nevada. Am J Obstet Gynecol 2019;221:B2-5.
    1. Finer LB, Zolna MR. Declines in unintended pregnancy in the United States, 2008-2011. N Engl J Med 2016;374:843-52.
    1. Practice Committees of American Society for Reproductive Medicine, Society for Assisted Reproductive Technology. Mature oocyte cryopreservation: a guideline. Fertil Steril 2013;99:37-43.

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