Neuromyelitis optica spectrum disorders and pregnancy: Interactions and management

Abstract

Neuromyelitis optica spectrum disorders (NMOSD) predominantly affect women who are of childbearing age. Understanding the interactions between pregnancy and NMOSD is important for clinical management. Aquaporin-4 (AQP4), the most common target antigen in NMOSD, is expressed on placenta in early pregnancy. A variety of immune and cytokine changes in pregnancy may impact pregnancy outcomes in NMOSD patients. Relapses continue during pregnancy and increase in frequency postpartum. Preeclampsia and fetal loss are more frequent in NMOSD than in controls. Transfer of AQP4-immunoglobulin G (IgG) from mother to baby occurs but appears not to cause disease. Several treatment options are relatively safe and mitigate the risk of relapse during pregnancy and postpartum. For patients with active NMOSD, it may be advisable to continue immunotherapy during pregnancy.

Keywords

NMOSD pregnancy relapse rate miscarriage immunosuppressive safety breast feeding

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References

Wingerchuk

Banwell

Bennett

et al

International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 2015; 85: 177–189.

Lennon

Wingerchuk

Kryzer

et al

A serum autoantibody marker of neuromyelitis optica: Distinction from multiple sclerosis. Lancet 2004; 364: 2106–2112.

Papadopoulos

Verkman

AS.

Aquaporin 4 and neuromyelitis optica. Lancet Neurol 2012; 11: 535–544.

Varrin-Doyer

Spencer

Schulze-Topphoff

et al

Aquaporin 4-specific T cells in neuromyelitis optica exhibit a Th17 bias and recognize clostridium ABC transporter. Ann Neurol 2012; 72: 53–64.

Ratelade

Zhang

Saadoun

et al

Neuromyelitis optica IgG and natural killer cells produce NMO lesions in mice without myelin loss. Acta Neuropathol 2012; 123: 861–872.

Wang

Dai

Qiu

et al

Interleukin-17-secreting T cells in neuromyelitis optica and multiple sclerosis during relapse. J Clin Neurosci 2011; 18: 1313–1317.

Flanagan

Cabre

Weinshenker

et al

Epidemiology of aquaporin-4 autoimmunity and neuromyelitis optica spectrum. Ann Neurol. Epub ahead of print 17 February 2016. DOI: 10.1002/ana.24617.

Pandit

Asgari

Apiwattanakul

et al

Demographic and clinical features of neuromyelitis optica: A review. Mult Scler 2015; 21: 845–853.

Confavreux

Hutchinson

Hours

et al

Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in multiple sclerosis group. N Engl J Med 1998; 339: 285–291.

10.

Davoudi

Keyhanian

Bove

et al

Immunology of neuromyelitis optica during pregnancy. Neurol Neuroimmunol Neuroinflamm 2016; 3: e288.

11.

Saito

Nakashima

Shima

et al

Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol 2010; 63: 601–610.

12.

Wang

Hao

et al

Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J Reprod Immunol 2010; 84: 164–170.

13.

Szarka

Rigo

Lazar Beko Molvarec

LGA

. Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array. BMC Immunol 2010; 11: 59.

14.

Torricelli

Bellisai

Novembri

et al

High levels of maternal serum IL-17 and activin A in pregnant women affected by systemic lupus erythematosus. Am J Reprod Immunol 2011; 66: 84–89.

15.

Chihara

Aranami

Sato

et al

Interleukin 6 signaling promotes anti-aquaporin 4 autoantibody production from plasmablasts in neuromyelitis optica. Proc Natl Acad Sci U S A 2011; 108: 3701–3706.

16.

Borzychowski

Croy

Chan

et al

Changes in systemic type 1 and type 2 immunity in normal pregnancy and pre-eclampsia may be mediated by natural killer cells. Eur J Immunol 2005; 35: 3054–3063.

17.

Keyhanian

Davoudi

Etemadifar

et al

Better prognosis of multiple sclerosis in patients who experienced a full-term pregnancy. Eur Neurol 2012; 68: 150–155.

18.

Airas

Saraste

Rinta

et al

Immunoregulatory factors in multiple sclerosis patients during and after pregnancy: Relevance of natural killer cells. Clin Exp Immunol 2008; 151: 235–243.

19.

Lachapelle

Miron

Hemmings

et al

Endometrial T, B, and NK cells in patients with recurrent spontaneous abortion. Altered profile and pregnancy outcome. J Immunol 1996; 156: 4027–4034.

20.

Bourdette

Yadav

B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. Curr Neurol Neurosci 2008; 8: 417–418.

21.

Panchanathan

Choubey

Murine BAFF expression is up-regulated by estrogen and interferons: Implications for sex bias in the development of autoimmunity. Mol Immunol 2013; 53: 15–23.

22.

Nakashima

Takahashi

Cree

et al

Transient increases in anti-aquaporin-4 antibody titers following rituximab treatment in neuromyelitis optica, in association with elevated serum BAFF levels. J Clin Neurosci 2011; 18: 997–998.

23.

Karpuzoglu

Phillips

Gogal

et al

IFN-gamma-inducing transcription factor, T-bet is upregulated by estrogen in murine splenocytes: Role of IL-27 but not IL-12. Mol Immunol 2007; 44: 1808–1814.

24.

Feng

Reder

Yanamandala

et al

Type I interferon signature is high in lupus and neuromyelitis optica but low in multiple sclerosis. J Neurol Sci 2012; 313: 48–53.

25.

Pauklin

Sernandez

Bachmann

et al

Estrogen directly activates AID transcription and function. J Exp Med 2009; 206: 99–111.

26.

De Falco

Cobellis

Torella

et al

Down-regulation of aquaporin 4 in human placenta throughout pregnancy. In Vivo 2007; 21: 813–817.

27.

Saadoun

Waters

Leite

et al

Neuromyelitis optica IgG causes placental inflammation and fetal death. J Immunol 2013; 191: 2999–3005.

28.

Pierdominici

Maselli

Colasanti

et al

Estrogen receptor profiles in human peripheral blood lymphocytes. Immunol Lett 2010; 132: 79–85.

29.

Tradtrantip

Ratelade

Zhang

et al

Enzymatic deglycosylation converts pathogenic neuromyelitis optica anti-aquaporin-4 immunoglobulin G into therapeutic antibody. Ann Neurol 2013; 73: 77–85.

30.

Quick

Cipolla

MJ.

Pregnancy-induced up-regulation of aquaporin-4 protein in brain and its role in eclampsia. FASEB J 2005; 19: 170–175.

31.

Matiello

Schaefer-Klein

Sun

et al

Aquaporin 4 expression and tissue susceptibility to neuromyelitis optica. JAMA Neurol 2013; 70: 1118–1125.

32.

Kebir

Kreymborg

Ifergan

et al

Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 2007; 13: 1173–1175.

33.

Uzawa

Mori

Arai

et al

Cytokine and chemokine profiles in neuromyelitis optica: Significance of interleukin-6. Mult Scler 2010; 16: 1443–1452.

34.

Warabi

Matsumoto

Hayashi

Interferon beta-1b exacerbates multiple sclerosis with severe optic nerve and spinal cord demyelination. J Neurol Sci 2007; 252: 57–61.

35.

Kim

Nakashima

et al

Influence of pregnancy on neuromyelitis optica spectrum disorder. Neurology 2012; 78: 1264–1267.

36.

Nour

Nakashima

Coutinho

et al

Pregnancy outcomes in aquaporin-4-positive neuromyelitis optica spectrum disorder. Neurology 2016; 86: 79–87.

37.

Fragoso

Adoni

Bichuetti

et al

Neuromyelitis optica and pregnancy. J Neurol 2013; 260: 2614–2619.

38.

Huang

Wang

Zhou

et al

Pregnancy in neuromyelitis optica spectrum disorder: A multicenter study from South China. J Neurol Sci 2017; 372: 152–156.

39.

Bourre

Marignier

Zephir

et al

Neuromyelitis optica and pregnancy. Neurology 2012; 78: 875–879.

40.

Shi

Zhao

Geng

et al

Effectiveness and safety of immunosuppressive therapy in neuromyelitis optica spectrum disorder during pregnancy. J Neurol Sci 2017; 377: 72–76.

41.

Asgari

Henriksen

Petersen

et al

Pregnancy outcomes in a woman with neuromyelitis optica. Neurology 2014; 83: 1576–1577.

42.

Shang

Liu

Neuromyelitis optica during pregnancy. Int J Gynaecol Obstet 2011; 115: 66–68.

43.

Shimizu

Fujihara

Ohashi

et al

Pregnancy-related relapse risk factors in women with anti-AQP4 antibody positivity and neuromyelitis optica spectrum disorder. Mult Scler 2016; 22: 1413–1420.

44.

Wingerchuk

Banwell

Bennett

et al

International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 2015; 85: 177–189.

45.

Jurewicz

Selmaj

Relapse of neuromyelitis optica during pregnancy—Treatment options and literature review. Clin Neurol Neurosurg 2015; 130: 159–161.

46.

Bove

Elsone

Alvarez

et al

Female hormonal exposures and neuromyelitis optica symptom onset in a multicenter study. Neurol Neuroimmunol Neuroinflamm 2017; 4: e339.

47.

Igel

Garretto

Robbins

et al

Neuromyelitis optica in pregnancy complicated by posterior reversible encephalopathy syndrome, eclampsia and fetal death. J Clin Med Res 2015; 7: 193–195.

48.

Magana

Matiello

Pittock

et al

Posterior reversible encephalopathy syndrome in neuromyelitis optica spectrum disorders. Neurology 2009; 72: 712–717.

49.

Ringelstein

Harmel

Distelmaier

et al

Neuromyelitis optica and pregnancy during therapeutic B cell depletion: Infant exposure to anti-AQP4 antibody and prevention of rebound relapses with low-dose rituximab postpartum. Mult Scler 2013; 19: 1544–1547.

50.

Gomori

Pal

Abraham

et al

Fetal development of membrane water channel proteins aquaporin-1 and aquaporin-4 in the human brain. Int J Dev Neurosci 2006; 24: 295–305.

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