Safety of anti-TNF therapy in inflammatory bowel disease during pregnancy

Expert Opinion on Drug Safety

Volumn 13, Issue 12, 2014, Pages 1699-1708

  Khan, Nabeel ^a   Asim, Hamna ^b   Lichtenstein, Gary R ^c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b AGA KHAN UNIVERSITY HOSPITAL   (Pakistan)

^c Division of Gastroenterology   (United States)

Author keywords

Adalimumab; Anti TNF; Biologic agent; Certolizumab; Crohn's disease; Golimumab; Inflammatory bowel disease; Infliximab; Pregnancy; Ulcerative colitis

Indexed keywords

ADALIMUMAB; CERTOLIZUMAB PEGOL; GOLIMUMAB; INFLIXIMAB; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; ANTIINFLAMMATORY AGENT; TUMOR NECROSIS FACTOR ALPHA;

DISEASE ACTIVITY; DRUG EFFICACY; DRUG SAFETY; HUMAN; INFLAMMATORY BOWEL DISEASE; NONHUMAN; PREGNANCY OUTCOME; PREGNANT WOMAN; REMISSION; REVIEW; RISK ASSESSMENT; TREATMENT OUTCOME; ANIMAL; ANTAGONISTS AND INHIBITORS; FEMALE; INFLAMMATORY BOWEL DISEASES; PREGNANCY;

ANIMALS; ANTI-INFLAMMATORY AGENTS; FEMALE; HUMANS; INFLAMMATORY BOWEL DISEASES; PREGNANCY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84912020334     PISSN: 14740338     EISSN: 1744764X     Source Type: Journal    
DOI: 10.1517/14740338.2014.973399     Document Type: Review

References (105)

1. Molodecky NA, Soon IS, Rabi DM, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012;142(1):46-54; e42
2. Vind I, Riis L, Jess T, et al. Increasing incidences of inflammatory bowel disease and decreasing surgery rates in Copenhagen City and County, 2003-2005: A population-based study from the Danish Crohn colitis database. Am J Gastroenterol 2006;101(6):1274-82
3. Loftus CG, Loftus EV Jr, Harmsen WS, et al. Update on the incidence and prevalence of Crohn's disease and ulcerative colitis in Olmsted County, Minnesota, 1940-2000. Inflamm Bowel Dis 2007;13(3):254-61
4. Bernstein CN, Wajda A, Svenson LW, et al. The epidemiology of inflammatory bowel disease in Canada: A populationbased study. Am J Gastroenterol 2006;101(7):1559-68
5. Andres PG, Friedman LS. Epidemiology and the natural course of inflammatory bowel disease. Gastroenterol Clin North Am 1999;28(2):255-81
6. Cosnes J, Gower-Rousseau C, Seksik P, Cortot A. Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology 2011;140(6):1785-94; e4
7. Kappelman MD, Rifas-Shiman SL, Kleinman K, et al. The prevalence and geographic distribution of Crohn's disease and ulcerative colitis in the United States. Clin Gastroenterol Hepatol 2007;5(12):1424-9
8. Loftus EV Jr. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology 2004;126(6):1504-17
9. Vernier-Massouille G, Balde M, Salleron J, et al. Natural history of pediatric Crohn's disease: A populationbased cohort study. Gastroenterology 2008;135(4):1106-13
10. Riis L, Vind I, Politi P, et al. Does pregnancy change the disease course A study in a European cohort of patients with inflammatory bowel disease. Am J Gastroenterol 2006;101(7):1539-45
11. Dominitz JA, Young JC, Boyko EJ. Outcomes of infants born to mothers with inflammatory bowel disease: A population-based cohort study. Am J Gastroenterol 2002;97(3):641-8
12. Mahadevan U, Sandborn WJ, Li DK, et al. Pregnancy outcomes in women with inflammatory bowel disease: A large community-based study from Northern California. Gastroenterology 2007;133(4):1106-12
13. Nguyen GC, Boudreau H, Harris ML, Maxwell CV. Outcomes of obstetric hospitalizations among women with inflammatory bowel disease in the United States. Clin Gastroenterol Hepatol 2009;7(3):329-34
14. Nørga°rd B, Fonager K, Sørensen HT, Olsen J. Birth outcomes of women with ulcerative colitis: A nationwide Danish cohort study. Am J Gastroenterol 2000;95(11):3165-70
15. Kornfeld D, Cnattingius S, Ekbom A. Pregnancy outcomes in women with inflammatory bowel disease-A population-based cohort study. Am J Obstet Gynecol 1997;177(4):942-6
16. Fonager K, Sørensen HT, Olsen J, et al. Pregnancy outcome for women with Crohn's disease: A follow-up study based on linkage between national registries. Am J Gastroenterol 1998;93(12):2426-30
17. Cornish J, Tan E, Teare J, et al. A metaanalysis on the influence of inflammatory bowel disease on pregnancy. Gut 2007;56(6):830-7
18. Naganuma M, Kunisaki R, Yoshimura N, et al. Conception and pregnancy outcome in women with inflammatory bowel disease: A multicentre study from Japan. J Crohn's Colitis 2011;5(4):317-23
19. Tiainen J, Matikainen M, Hiltunen KM. Ileal J-pouch-Anal anastomosis, sexual dysfunction, and fertility. Scand J Gastroenterol 1999;34(2):185-8
20. Johnson P, Richard C, Ravid A. Female infertility after ileal pouch-Anal anastomosis for ulcerative colitis. Dis Colon Rectum 2004;47(7):1119-26
21. De Felice KM, Kane SV. Inflammatory bowel disease in women of reproductive age. Expert Rev Gastroenterol Hepatol 2014;8(4):417-25
22. Khosla R, Willoughby CP, Jewell DP. Crohn's disease and pregnancy. Gut 1984;25(1):52-6
23. Woolfson K, Cohen Z, McLeod RS. Crohn's disease and pregnancy. Dis Colon Rectum 1990;33(10):869-73
24. Hanan IM, Kirsner JB. Inflammatory bowel disease in the pregnant woman. Clin Perinatol 1985;12(3):669-82
25. Morales M, Berney T, Jenny A, et al. Crohn's disease as a risk factor for the outcome of pregnancy. Hepatogastroenterology 1999;47(36):1595-8
26. Mogadam M, Dobbins WO III, Korelitz BI, Ahmed SW. Pregnancy in Inflammatory Bowel Disease: effect of Sulfasalazine and Corticosteroids on Fetal Outcome. Gastroenterology 1981;80:72-6
27. Ujihara M, Ando T, Ishiguro K, et al. Importance of appropriate pharmaceutical management in pregnant women with ulcerative colitis. BMC Res Notes 2013;6(1):210
28. Getahun D, Fassett MJ, Longstreth GF, et al. Association between maternal inflammatory bowel disease and adverse perinatal outcomes. J Perinatol 2014;34(6):435-40
29. Friedman S. Medical therapy and birth outcomes in women with Crohn's disease: what should we tell our patients Am J Gastroenterol 2007;102(7):1414-16
30. Katz JA, Pore G. Inflammatory bowel disease and pregnancy. Inflamm Bowel Dis 2001;7(2):146-57
31. Castiglione F, Pignata S, Morace F, et al. Effect of pregnancy on the clinical course of a cohort of women with inflammatory bowel disease. Ital J Gastroenterol 1996;28(4):199-204
32. Kane S, Kisiel J, Shih L, Hanauer S. HLA disparity determines disease activity through pregnancy in women with inflammatory bowel disease. Am J Gastroenterol 2004;99(8):1523-6
33. Calderwood AH, Kane SV. Gastroenterology expert column: IBD and pregnancy. MedGenMed 2004;6(4):14
34. Baird D, Narendranathan M, Sandler RS. Increased risk of preterm birth for women with inflammatory bowel disease. Gastroenterology 1990;99(4):987-94
35. Mayberry J, Weterman I. European survey of fertility and pregnancy in women with Crohn's disease: A case control study by European Collaborative Group. Gut 1986;27(7):821-5
36. Marri SR, Ahn C, Buchman AL. Voluntary childlessness is increased in women with inflammatory bowel disease. Inflamm Bowel Dis 2007;13(5):591-9
37. Van Assche G, Dignass A, Reinisch W, et al. European Crohn's and Colitis Organisation (ECCO). The second European evidence-based consensus on the diagnosis and management of Crohn's disease: special situations. J Crohn's Colitis 2010;4(1):63-101
38. Selinger CP, Eaden J, Selby W, et al. Inflammatory bowel disease and pregnancy: lack of knowledge is associated with negative views. J Crohn's Colitis 2013;7(6):e206-13
39. Selinger CP, Eaden J, Selby W, et al. Patients' knowledge of pregnancy-related issues in inflammatory bowel disease and validation of a novel assessment tool ('CCPKnow'). Aliment Pharmacol Ther 2012;36(1):57-63
40. Selinger CP, Leong RW, Lal S. Pregnancy related issues in inflammatory bowel disease: evidence base and patients' perspective. World J Gastroenterol 2012;18(21):2600
41. Administration, US F.A.D. FDA Pregnancy categories. FDA; editor
42. Rutgeerts P, Assche G, Vermeire S. Review article: infliximab therapy for inflammatory bowel disease-seven years on. Aliment Pharmacol Ther 2006;23(4):451-63
43. Katz JA, Antoni C, Keenan GF, et al. Outcome of pregnancy in women receiving infliximab for the treatment of Crohn's disease and rheumatoid arthritis. Am J Gastroenterol 2004;99(12):2385-92
44. Ventura SJ, Mosher WD, Curtin SC, et al. Trends in pregnancy rates for the United States, 1976-97: An update. Natl Vital Stat Rep 2001;49(4):1-12
45. Hudson M, Flett G, Sinclair TS, et al. Fertility and pregnancy in inflammatory bowel disease. Int J Gynecol Obstet 1997;58(2):229-37
46. Lichtenstein GR, Feagan BG, Cohen RD, et al. Serious infections and mortality in association with therapies for Crohn's disease: TREAT registry. Clin Gastroenterol Hepatol 2006;4(5):621-30
47. Mahadevan U, Kane S, Sandborn WJ, et al. Intentional infliximab use during pregnancy for induction or maintenance of remission in Crohn's disease. Aliment Pharmacol Ther 2005;21(6):733-8
48. Lichtenstein GR, Feagan BG, Cohen RD, et al. Serious infection and mortality in patients with Crohn's disease: more than 5 years of follow-up in the TREAT-registry. Am J Gastroenterol 2012;107(9):1409-22
49. Mahadevan U, Martin CF, Chambers C, et al. 1 Achievement of developmental milestones among offspring of women with inflammatory bowel disease: the PIANO registry. Gastroenterology 2014;146(5):S-1
50. Mahadevan U, Martin CF, Sandler RS, et al. 764 one year newborn outcomes among offspring of women with inflammatory bowel disease: the PIANO registry. Gastroenterology 2010;138(5):S-106
51. Mahadevan U, Martin CF, Sandler RS, et al. 865 PIANO: A 1000 patient prospective registry of pregnancy outcomes in women with IBD exposed to immunomodulators and biologic therapy. Gastroenterology 2012;142(5):S-149
52. Schnitzler F, Fidder H, Ferrante M, et al. Outcome of pregnancy in women with inflammatory bowel disease treated with antitumor necrosis factor therapy. Inflamm Bowel Dis 2011;17(9):1846-54
53. Arguëlles-Arias F, Castro-Laria L, Barreiro-de Acosta M, et al. Is safety infliximb during pregnancy in patients with inflammatory bowel disease Rev Esp Enferm Dig 2012;104(2):59
54. Carter JD, Ladhani A, Ricca LR, et al. A safety assessment of tumor necrosis factor antagonists during pregnancy: A review of the Food and Drug Administration database. J Rheumatol 2009;36(3):635-41
55. Yarur A, Kane SV. Update on pregnancy and breastfeeding in the era of biologics. Dig Liver Dis 2013;45(10):787-94
56. Joven BE, Garcia-Gonzalez AJ, Ruiz T, et al. Pregnancy in women receiving anti-TNF-Alpha therapy. Experience in Spain. Arthritis Rheum 2005;52(9):S349-S349
57. Hyrich KL, Symmons DP, Watson KD, et al. Pregnancy outcome in women who were exposed to anti-tumor necrosis factor agents: results from a national population register. Arthritis Rheum 2006;54(8):2701-2
58. Berthelot JM, De Bandt M, Goupille P, et al. Exposition to anti-TNF drugs during pregnancy: outcome of 15 cases and review of the literature. Joint Bone Spine 2009;76(1):28-34
59. Angelucci E, Cocco A, Viscido A, Caprilli R. Safe use of infliximab for the treatment of fistulizing Crohn's disease during pregnancy within 3 months of conception. Inflamm Bowel Dis 2008;14(3):435-6
60. Rosner I, Haddad A, Boulman N, et al. Pregnancy in rheumatology patients exposed to anti-tumour necrosis factor (TNF)-Alpha therapy. Rheumatology 2007;46(9):1508-8
61. Verstappen SM, King Y, Watson KD, et al. Anti-TNF therapies and pregnancy: outcome of 130 pregnancies in the British Society for Rheumatology Biologics Register. Ann Rheum Dis 2011;70(5):823-6
62. Zelinkova Z, de Haar C, de Ridder L, et al. High intra-uterine exposure to infliximab following maternal anti-TNF treatment during pregnancy. Aliment Pharmacol Ther 2011;33(9):1053-8
63. Vinet E, Pineau C, Gordon C, et al. Biologic therapy and pregnancy outcomes in women with rheumatic diseases. Arthritis Care Res 2009;61(5):587-92
64. 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(1):228-33
65. Simister NE. Placental transport of immunoglobulin G. Vaccine 2003;21(24):365-3369
66. Panaccione R, Fedorak RN, Aumais G, et al. Review and clinical perspectives for the use of infliximab in ulcerative colitis. Can J Gastroenterol 2008;22(3):261
67. Mahadevan U, Wolf DC, Dubinsky M, et al. Placental Transfer of Anti-Tumor Necrosis Factor Agents in Pregnant Patients With Inflammatory Bowel Disease. Clin Gastroenterol Hepatol 2013;11(3):286-92
68. Mahadevan U, Martin CF, Dubinsky M, et al. 960 exposure to anti-TNF-Alpha therapy in the third trimester of pregnancy is not associated with increased adverse outcomes: results from the PIANO registry. Gastroenterology 2014;146(5):S-170
69. Mahadevan U, Kane SV, Church JA, et al. 499 the effect of maternal peripartum infliximab use on neonatal immune response. Gastroenterology 2008;134(4):A-69
70. Vasiliauskas EA, Church JA, Silverman N, et al. Case report: evidence for transplacental transfer of maternally administered infliximab to the newborn. Clin Gastroenterol Hepatol 2006;4(10):1255-8
71. Gisbert JP. Safety of immunomodulators and biologics for the treatment of inflammatory bowel disease during pregnancy and breast-feeding. Inflamm Bowel Dis 2010;16(5):881-95
72. Kane S, Ford J, Cohen R, Wagner C. Absence of infliximab in infants and breast milk from nursing mothers receiving therapy for Crohn's disease before and after delivery. J Clin Gastroenterol 2009;43(7):613-16
73. Stengel JZ, Arnold HL. Is infliximab safe to use while breastfeeding World J Gastroenterol 2008;14(19):3085
74. Peltier M, James D, Ford J, et al. Infliximab levels in breast-milk of a nursing Crohn's patient. Am J Gastroenterol 2001;96(9):S312
75. Fritzsche J, Pilch A, Mury D, et al. Infliximab and adalimumab use during breastfeeding. J Clin Gastroenterol 2012;46(8):718-19
76. Mahadevan U, Cucchiara S, Hyams JS, et al. The London position statement of the World Congress of gastroenterology on biological therapy for IBD with the European crohn's and colitis Organisation: pregnancy and pediatrics. Am J Gastroenterol 2011;106(2):214-23
77. Moffatt DC, Bernstein CN. Drug therapy for inflammatory bowel disease in pregnancy and the puerperium. Best Pract Res Clin Gastroenterol 2007;21(5):835-47
78. Ben-Horin S, Yavzori M, Katz L, et al. Adalimumab level in breast milk of a nursing mother. Clin Gastroenterol Hepatol 2010;8(5):475-6
79. Ben-Horin S, Yavzori M, Kopylov U, et al. Detection of infliximab in breast milk of nursing mothers with inflammatory bowel disease. J Crohn's Colitis 2011;5(6):555-8
80. Djokanovic N, Klieger-Grossmann C, Pupco A, Koren G. Safety of infliximab use during pregnancy. Reprod Toxicol 2011;32(1):93-7
81. Colombel JF. Efficacy and safety of adalimumab for the treatment of Crohn's disease in adults. Expert Rev Gastroenterol Hepatol 2008;2(2):163-76
82. Colombel JF, Sandborn WJ, Rutgeerts P, et al. Adalimumab for maintenance of clinical response and remission in patients with Crohn's disease: the CHARM trial. Gastroenterology 2007;132(1):52-65
83. Sandborn WJ, Rutgeerts P, Enns R, et al. Adalimumab induction therapy for Crohn disease previously treated with infliximab: A randomized trial. Ann Intern Med 2007;146(12):829-38
84. Vesga L, Terdiman J, Mahadevan U. Adalimumab use in pregnancy. Gut 2005;54(6):890-0
85. Coburn LA, Wise PE, Schwartz DA. The successful use of adalimumab to treat active Crohn's disease of an ileoanal pouch during pregnancy. Dig Dis Sci 2006;51(11):2045-7
86. Roux CH, Brocq O, Breuil V, et al. Pregnancy in rheumatology patients exposed to anti-tumour necrosis factor (TNF)-Alpha therapy. Rheumatology 2007;46(4):695-8
87. Sánchez Munõz D, Hoyas Pablos E, Ramrez Martn Del Campo M, et al. Term pregnancy in a patient with Crohn's disease under treatment with adalimumab. Gastroenterol Hepatol 2005;28(7):435
88. Weber-Schoendorfer C, Fritzsche J, Schaefer C. Pregnancy outcomes in women exposed to adalimumab or infliximab: the experience of the Berlin Institute for Clinical teratology and drug risk assessment in pregnancy. Reprod Toxicol 2011;31(2):267-8
89. Chambers CD, Johnson DL. Emerging data on the use of anti-tumor necrosis factor-Alpha medications in pregnancy. Birth Defects Res A Clin Mol Teratol 2012;94(8):607-11
90. Johnson DL, Jones KL, Chambers CD, Salas E. 142 Pregnancy Outcomes in Women Exposed to Adalimumab: the OTIS Autoimmune Diseases in Pregnancy Project. Gastroenterology 2009;136(5):A-27 .
91. Mahadevan U, Kane S. American Gastroenterological Association Institute medical position statement on the use of gastrointestinal medications in pregnancy. Gastroenterology 2006;131(1):278-82
92. Pasut G. Pegylation of biological molecules and potential benefits: pharmacological properties of certolizumab pegol. BioDrugs 2014;28(1):15-23
93. Weir N, Athwal D, Brown D, et al. A new generation of high-Affinity humanized PEGylated Fab fragment anti-tumor necrosis factor-Alpha monoclonal antibodies. Future Med 2006;3(4):535-45
94. Wakefield I, Stephens S, Foulkes R, et al. The use of surrogate antibodies to evaluate the developmental and reproductive toxicity potential of an anti-TNFalpha PEGylated Fab¢ monoclonal antibody. Toxicol Sci 2011;122(1):170-6
95. Hassid B, Mahadevan U. The use of biologic therapy in pregnancy: A gastroenterologist's perspective. Curr Opin Rheumatol 2014;26(3):347-53
96. Oussalah A, Bigard M, Peyrin-Biroulet L. Certolizumab use in pregnancy. Gut 2009;58(4):608
97. Steinberg SA, Ullman TA. W1318 certolizumab treatment of linear IgA dermatosis in a pregnant crohn's colitis patient: A case study and review of the literature. Gastroenterology 2010;138(5):S-698
98. Mahadevan U, Vermelre S, Wolf DC, et al. DOP024 Pregnancy outcomes after exposure to certolizumab pegol: results from safety surveillance. J Crohn's Colitis 2014;8:S26
99. Ventura SJ, Abma JC, Mosher WD. Estimated pregnancy rates by outcome for the United States, 1990-2004. US Department of Health & Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics. Natl Vital Stat Rep 2008;56(15):1-25
100. Clowse ME, Wolf DC, Forger F, et al. Retrospective analysis of certolizumab pegol use during pregnancy: update of impact on birth outcomes. In: Arthritis and rheumatism. Wiley-Blackwell; 111 River st, Hoboken 07030-5774, NJ USA: 2013
101. Porter C, Kopotsha T, Smith BJ, et al. No significant transfer of certolizumab pegol compared with IgG in the perfused human placenta in vitro. Ann Rheum Dis 2010;69(Suppl 3):210
102. Wolf D, Mahadevan U. Certolizumab pegol use in pregnancy: low levels detected in cord blood. Arthr Rheum 2010;62(Suppl 10):299
103. Mahadevan U, Abreu MT. 960 certolizumab use in pregnancy: low levels detected in cord blood. Gastroenterology 2009;136(5):A-146
104. Lau AG, Clark M, Harrison DD, et al. Pregnancy outcomes in women exposed to golimumab. In: Arthritis and rheumatism. Wiley-BlackWell; 111 River ST, Hoboken 07030-5774, NJ USA: 2013
105. Martin PL, Oneda S, Reacy G. Effects of an anti-TNF-Alpha monoclonal antibody, administered throughout pregnancy and lactation, on the development of the macaque immune system. Am J Reprod Immunol 2007;58(2):138-49