Safety of TNF-α inhibitors during IBD pregnancy: A systematic review

BMC Medicine

Volumn 11, Issue 1, 2013, Pages

  Nielsen, Ole Haagen ^a   Loftus, Edward V ^b   Jess, Tine ^c  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b MAYO CLINIC   (United States)

^c STATENS SERUM INSTITUT   (Denmark)

Author keywords

Biologics; Crohn's disease; IBD; Lactation; Pregnancy; Ulcerative colitis

Indexed keywords

ADALIMUMAB; CERTOLIZUMAB PEGOL; GOLIMUMAB; INFLIXIMAB; METHOTREXATE; TUMOR NECROSIS FACTOR ALPHA INHIBITOR;

ADVERSE OUTCOME; ARTICLE; CONGENITAL MALFORMATION; DRUG SAFETY; ENTERITIS; FEMALE; FETUS DISEASE; HUMAN; INFECTION RISK; INFORMATION RETRIEVAL; LOW BIRTH WEIGHT; OUTCOME ASSESSMENT; POLYDACTYLY; PREGNANCY COMPLICATION; PREGNANCY OUTCOME; PREGNANT WOMAN; PREMATURE LABOR; PREMATURITY; RISK ASSESSMENT; SPONTANEOUS ABORTION; STILLBIRTH; SYSTEMATIC REVIEW; TERATOGENESIS; THIRD TRIMESTER PREGNANCY;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; FEMALE; HUMANS; INFLAMMATORY BOWEL DISEASES; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY OUTCOME; PRENATAL EXPOSURE DELAYED EFFECTS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84880949345     PISSN: None     EISSN: 17417015     Source Type: Journal    
DOI: 10.1186/1741-7015-11-174     Document Type: Article

References (94)

1. Cornish J, Tan E, Teare J, Teoh TG, Rai R, Clark SK, Tekkis PP. A meta-analysis on the influence of inflammatory bowel disease on pregnancy. Gut 2007, 56:830-837. 1954859, 17185356.
2. Bortoli A, Saibeni S, Tatarella M, Prada A, Beretta L, Rivolta R, Politi P, Ravelli P, Imperiali G, Colombo E, Pera A, Daperno M, Carnovali M, de Franchis R, Vecchi M. Pregnancy before and after the diagnosis of inflammatory bowel diseases: retrospective case-control study. J Gastroenterol Hepatol 2007, 22:542-549.
3. Fonager K, Sorensen HT, Olsen J, Dahlerup JF, Rasmussen SN. Pregnancy outcome for women with Crohn's disease: a follow-up study based on linkage between national registries. Am J Gastroenterol 1998, 93:2426-2430.
4. Nielsen OH, Andreasson B, Bondesen S, Jarnum S. Pregnancy in ulcerative colitis. Scand J Gastroenterol 1983, 18:735-742.
5. Nielsen OH, Andreasson B, Bondesen S, Jacobsen O, Jarnum S. Pregnancy in Crohn's disease. Scand J Gastroenterol 1984, 19:724-732.
6. Ferguson CB, Mahsud-Dornan S, Patterson RN. Inflammatory bowel disease in pregnancy. BMJ 2008, 337:a427. 2483894, 18599468.
7. Mahadevan U, Kane S. American Gastroenterological Association Institute technical review on the use of gastrointestinal medications in pregnancy. Gastroenterology 2006, 131:283-311.
8. Nielsen OH, Seidelin JB, Munck LK, Rogler G. Use of biological molecules in the treatment of inflammatory bowel disease. J Intern Med 2011, 270:15-28.
9. Pregnancy categories 2012, http://labels.fda.gov/ingredientname.cfm.
10. Nielsen OH, Jess T. IBD: Can TNF inhibitors be administered during the third trimester?. Nat Rev Gastroenterol Hepatol 2012, 10:130-131.
11. Chaparro M, Gisbert JP. Transplacental transfer of immunosuppressants and biologics used for the treatment of inflammatory bowel disease. Curr Pharm Biotechnol 2011, 12:765-773.
12. Zelinkova Z, van der Ent C, Bruin KF, van Baalen O, Vermeulen HG, Smalbraak HJ, Ouwendijk RJ, Hoek AC, van der Werf SD, Kuipers EJ, van der Woude CJ. Effects of discontinuing anti-tumor necrosis factor therapy during pregnancy on the course of inflammatory bowel disease and neonatal exposure. Clin Gastroenterol Hepatol 2013, 11:318-321.
13. Friedman S, Regueiro MD. Pregnancy and nursing in inflammatory bowel disease. Gastroenterol Clin North Am 2002, 31:265-273.
14. Hou JK, Mahadevan U. A 24-year-old pregnant woman with inflammatory bowel disease. Clin Gastroenterol Hepatol 2009, 7:944-947.
15. Oussalah A, Roblin X, Laharie D, Filippi J, Flamant M, Faure P, Phelip JM, Bigard MA, Peyrin-Biroulet L. Tumour necrosis factor antagonists and inflammatory bowel diseases: a national practice survey. Aliment Pharmacol Ther 2009, 30:854-863.
16. Vasiliauskas EA, Church JA, Silverman N, Barry M, Targan SR, Dubinsky MC. Case report: evidence for transplacental transfer of maternally administered infliximab to the newborn. Clin Gastroenterol Hepatol 2006, 4:1255-1258.
17. Mahadevan U, Wolf DC, Dubinsky M, Cortot A, Lee SD, Siegel CA, Ullman T, Glover S, Valentine JF, Rubin DT, Miller J, Abreu MT. Placental transfer of anti-tumor necrosis factor agents in pregnant patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 2013, 11:286-292.
18. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) Group. JAMA 2000, 283:2008-2012.
19. Slama W, Roc E, Carlier P, Garayt C, Theophile H, Boyer M, et al. Pregnancy outcome in women exposed to anti tumor necrosis factor therapy. Congres de Physiologie, de Pharmacologie et de Therapeutique, Bordeaux, March 23-25, 2010 2010, 89. Oxford: Blackwell Publishing Ltd.
20. Palmer RB, Poullis AP, Pollok RCG. Acute severe colitis in pregnancy treated with infliximab http://www.gastrohep.com/classcases/classcases.asp?id=35.
21. Srinivasan R. Infliximab treatment and pregnancy outcome in active Crohn's disease. Am J Gastroenterol 2001, 96:2274-2275.
22. Steenholdt C, Al-Khalaf M, Ainsworth MA, Brynskov J. Therapeutic infliximab drug level in a child born to a woman with ulcerative colitis treated until gestation week 31. J Crohns Colitis 2012, 6:358-361.
23. Arai K, Takeuchi Y, Oishi C, Imawari M. The impact of disease activity of Crohn's disease during pregnancy on fetal growth. Clin J Gastroenterol 2010, 3:179-181.
24. Bank L, Hunt B. Unexpected dramatic clinical response of psoriasis lesions and unexpected pregnancy in an infertile patient in response to treatment with anti-tumor necrosis factor monoclonal antibody for Crohn's disease. Am J Gastroenterol 2002, 97:S260.
25. James RL, Pearson LL. Successful treatment of pregnancy-triggered Crohn's disease complicated by severe recurrent life-threatening gastrointestinal bleeding. Am J Gastroenterol 2001, 96:S295.
26. 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, 14:435-436.
27. Burt MJ, Frizelle FA, Barbezat GO. Pregnancy and exposure to infliximab (anti-tumor necrosis factor-alpha monoclonal antibody). J Gastroenterol Hepatol 2003, 18:465-466.
28. Mahadevan U, Terdiman JP, Church J, Vasiliauskas E, Gitis A, Dubinsky MC. Infliximab levels in infants born to women with inflammatory bowel disease. Gastroenterology 2007, 132:A-144.
29. Malgarinos G, Gikas A, Delicha E, Stamataki A, Georgopoulos F, Papadimitriou A, Stanciu C, Triantafillidis JK. Pregnancy and inflammatory bowel disease: a prospective case-control study. Rev Med Chir Soc Med Nat Iasi 2007, 111:613-619.
30. Correia LM, Bonilha DQ, Ramos JD, Ambrogini O, Miszputen SJ. Inflammatory bowel disease and pregnancy: report of two cases treated with infliximab and a review of the literature. Eur J Gastroenterol Hepatol 2010, 22:1260-1264.
31. 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, 104:228-233.
32. Mahadevan U, Kane S, Sandborn WJ, Cohen RD, Hanson K, Terdiman JP, Binion DG. Intentional infliximab use during pregnancy for induction or maintenance of remission in Crohn's disease. Aliment Pharmacol Ther 2005, 21:733-738.
33. Stengel JZ, Arnold HL. Is infliximab safe to use while breastfeeding?. World J Gastroenterol 2008, 14:3085-3087. 2712180, 18494064.
34. Tursi A. Effect of intentional infliximab use throughout pregnancy in inducing and maintaining remission in Crohn's disease. Dig Liver Dis 2006, 38:439-440.
35. Casanova MJ, Chaparro M, Domenech E, Barreiro-de AM, Bermejo F, Iglesias E, Gomollon F, Rodrigo L, Calvet X, Esteve M, Garcia-Planella E, Garcia-Lopez S, Taxonera C, Calvo M, Lopez M, Ginard D, Gomez-Garcia M, Garrido E, Perez-Calle JL, Beltran B, Piqueras M, Saro C, Botella B, Duenas C, Ponferrada A, Manosa M, Garcia-Sanchez V, Mate J, Gisbert JP. Safety of thiopurines and anti-TNF-alpha drugs during pregnancy in patients with inflammatory bowel disease. Am J Gastroenterol 2013, 108:433-440.
36. Lichtenstein GR, Feagan BG, Cohen RD, Salzberg BA, Diamond RH, Price S, Langholff W, Londhe A, Sandborn WJ. 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, 107:1409-1422. 3438468, 22890223.
37. Habal F. Biologic therapy in pregnancy and inflammatory bowel disease: a prospective 7 year study: clinical outcome. J Crohns Colitis 2013, 7:S243.
38. Snoeckx Y, Clark M, Geldhof A, Morgan J, Nissinen R, Schlegelmilch J. Pregnancy outcomes in women with inflammatory bowel disease exposed to infliximab. J Crohns Colitis 2013, 7:S170.
39. Traussnigg S, Eser A, Primas C, Papay P, Gratzer C, Angelberger S, Mikulits A, Reinisch W, Trauner M, Vogelsang H, Novacek G, Dejaco C. Adalimumab and infliximab therapy during pregnancy in IBD: a prospective assessment of outcome, safety and cord blood levels. J Crohns Colitis 2013, 7:S252.
40. Abdul Wahab NA, Milner M. Inflammatory bowel disease in pregnancy: report of a case treated with infliximab and litterature review. Ir J Med Sci 2011, 180:S131-S132.
41. Kozeluhova J. Biological treatment of patient with ulcerative colitis during pregnancy. Cesk Sloven Gastroent Hepatol 2011, 65:75-77.
42. Arguelles-Arias F, Castro-Laria L, Barreiro-de AM, Garcia-Sanchez MV, Guerrero-Jimenez P, Gomez-Garcia MR, Cordero-Ruiz P, Iglesias-Flores E, Gomez-Camacho F, Dominguez-Munoz EJ. Is safety infliximb during pregnancy in patients with inflammatory bowel disease?. Rev Esp Enferm Dig 2012, 104:59-64.
43. Machková N, Bortlik M, Duricova D, Bouzkova E, Lukas M. Pregnancy and newborn outcome of mothers with inflammatory bowel disease exposed to anti-TNF-alpha therapy during pregnancy. J Crohns Colitis 2012, 6:S157.
44. Aratari A, Margagnoni G, Koch M, Papi C. Intentional infliximab use during pregnancy for severe steroid-refractory ulcerative colitis. J Crohns Colitis 2011, 5:262.
45. Chaparro M, Gisbert JP. Successful use of infliximab for perianal Crohn's disease in pregnancy. Inflamm Bowel Dis 2011, 17:868-869.
46. Dunne C, Keegan D, Alakkari A, O'Donoghue D, Mulcahy H, Doherty GA. Pretty baby: successful use of anti-TNF-alpha therapy for Crohn's disease in pregnancy. J Crohns Colitis 2011, 5:S122.
47. Molnar T, Farkas K, Nagy F, Lakatos PL, Miheller P, Nyari T, Horvath G, Szepes Z, Marik A, Wittmann T. Pregnancy outcome in patients with inflammatory bowel disease according to the activity of the disease and the medical treatment: a case-control study. Scand J Gastroenterol 2010, 45:1302-1306.
48. Casanova MJ, Chaparro M, Flores EI, Rodrigo L, Mate J, Gisbert JP. Safety of immunomodulators and anti-TNF drugs for the treatment of inflammatory bowel disease during pregnancy. Gastroenterology 2011, 140:S-266.
49. Katz JA, Antoni C, Keenan GF, Smith DE, Jacobs SJ, Lichtenstein GR. Outcome of pregnancy in women receiving infliximab for the treatment of Crohn's disease and rheumatoid arthritis. Am J Gastroenterol 2004, 99:2385-2392.
50. Zelinkova Z, de Haar C, de Ridder L, Pierik MJ, Kuipers EJ, Peppelenbosch MP, van der Woude CJ. High intra-uterine exposure to infliximab following maternal anti-TNF treatment during pregnancy. Aliment Pharmacol Ther 2011, 33:1053-1058.
51. Mahadevan U, Martin CF, Sandler RS, Kane S, Dubinsky MC, Lewis JD, Sandborn WJ, Sands BE. PIANO: a 1000 patient prospective registry of pregnancy outcomes in women with IBD exposed to immunomodulators and biologic therapy. Updated presentation at the DDW 2012. Gastroenterology 2012, 142:S-149.
52. Seirafi M, Treton X, de Vroey B, Cosnes J, Roblin X, Allez M, Marteau P, Biroulet LP, Bouhnik Y. Anti-TNF therapy and pregnancy in inflammatory bowel disease: a prospective cohort study from the GETAID. Gastroenterology 2011, 140:S-175.
53. Mahadevan U. Management of your pregnant IBD patients. AGA Spring Postgraduate Course 2013, May, 18-19:367-379.
54. Schnitzler F, Fidder H, Ferrante M, Ballet V, Noman M, Van AG, Spitz B, Hoffman I, Van SK, Vermeire S, Rutgeerts P. Outcome of pregnancy in women with inflammatory bowel disease treated with antitumor necrosis factor therapy. Inflamm Bowel Dis 2011, 17:1846-1854.
55. Vinet E, Pineau C, Gordon C, Clarke AE, Bernatsky S. Biologic therapy and pregnancy outcomes in women with rheumatic diseases. Arthritis Rheum 2009, 61:587-592.
56. Carter JD, Ladhani A, Ricca LR, Valeriano J, Vasey FB. A safety assessment of tumor necrosis factor antagonists during pregnancy: a review of the Food and Drug Administration database. J Rheumatol 2009, 36:635-641.
57. Sandborn WJ, Hanauer SB, Katz S, Safdi M, Wolf DG, Baerg RD, Tremaine WJ, Johnson T, Diehl NN, Zinsmeister AR. Etanercept for active Crohn's disease: a randomized, double-blind, placebo-controlled trial. Gastroenterology 2001, 121:1088-1094.
58. Koren G, Inoue M. Do tumor necrosis factor inhibitors cause malformations in humans?. J Rheumatol 2009, 36:465-466.
59. Winger EE, Reed JL. Was risk properly assessed in Carter, et al's safety assessment of tumor necrosis factor antagonists during pregnancy?. J Rheumatol 2009, 36:2122.
60. Solomon BD. VACTERL/VATER Association. Orphanet J Rare Dis 2011, 6:56. 3169446, 21846383.
61. O'Donnell S, O'Morain C. Review article: use of antitumour necrosis factor therapy in inflammatory bowel disease during pregnancy and conception. Aliment Pharmacol Ther 2008, 27:885-894.
62. Mahadevan U, Cucchiara S, Hyams JS, Steinwurz F, Nuti F, Travis SP, Sandborn WJ, Colombel JF. 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, 106:214-223.
63. Cheent K, Nolan J, Shariq S, Kiho L, Pal A, Arnold J. Case Report: Fatal case of disseminated BCG infection in an infant born to a mother taking infliximab for Crohn's disease. J Crohns Colitis 2010, 4:603-605.
64. Xirouchakis E, Karantanos P, Tsartsali L, Karkatzos E. Pregnancy and Crohn's disease: Infliximab induction therapy, accidental conception, pregnancy outcome and postpartum complications. Ann Gastroenterol 2006, 19:138-140.
65. Angelucci E, Cesarini M, Vernia P. Inadvertent conception during concomitant treatment with infliximab and methotrexate in a patient with Crohn's disease: is the game worth the candle?. Inflamm Bowel Dis 2010, 16:1641-1642.
66. Epping G, van der Valk PD, Hendrix R. Legionella pneumophila pneumonia in a pregnant woman treated with anti-TNF-alpha antibodies for Crohn's disease: a case report. J Crohns Colitis 2010, 4:687-689.
67. Naganuma M, Kunisaki R, Yoshimura N, Nagahori M, Yamamoto H, Kimura H, Sako M, Kawaguchi T, Takazoe M, Yamamoto S, Matsui T, Hibi T, Watanabe M. Conception and pregnancy outcome in women with inflammatory bowel disease: A multicentre study from Japan. J Crohns Colitis 2011, 5:317-323.
68. 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, 43:613-616.
69. Mahadevan U, Martin CF, Sandler RS, Kane SV, Dubinsky MC, Lewis JD, Sandborn WJ, Sands BE. One year newborn outcomes among offspring of women with inflammatory bowel disease: The PIANO Registry. Gastroenterology 2010, 138:S-106.
70. Baker DE. Adalimumab: human recombinant immunoglobulin g1 anti-tumor necrosis factor monoclonal antibody. Rev Gastroenterol Disord 2004, 4:196-210.
71. Bosworth BP, Inra J, Eswaran S, Scherl EJ. Failed use of adalimumab in maintaining remission in Crohn's disease during pregnancy. Am J Gastroenterol 2007, 102:S322.
72. Johnson DL, Jones KL, Jimenez J, Mirrasoul BA, Salas E, Chambers CD. Pregnancy outcomes in women exposed to adalimumab: the OTIS autoimmune diseases in pregnancy project. Am J Gastroenterol 2009, 104:S410.
73. Abdul Wahab NA, Harkin R. Humira in pregnancy for Crohn's disease: a case report. Ir J Med Sci 2011, 180:S132.
74. Ben-Horin S, Yavzori M, Katz L, Picard O, Fudim E, Chowers Y, Lang A. Adalimumab level in breast milk of a nursing mother. Clin Gastroenterol Hepatol 2010, 8:475-476.
75. Chambers CD, Johnson DL, Jones KL. Adalimumab and pregnancy outcome: The OTIS autoimmune disease in pregnancy project. Am J Gastroenterol 2006, 101:S421-S422.
76. Mahadevan U, Miller JK, Wolf DC. Adalimumab levels detected in cord blood and infants exposed in utero. Gastroenterology 2011, 140:S61-S62.
77. 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, 51:2045-2047.
78. Jürgens M, Brand S, Filik L, Hubener C, Hasbargen U, Beigel F, Tillack C, Goke B, Ochsenkuhn T, Seiderer J. Safety of adalimumab in Crohn's disease during pregnancy: case report and review of the literature. Inflamm Bowel Dis 2010, 16:1634-1636.
79. Mishkin DS, Van DW, Becker JM, Farraye FA. Successful use of adalimumab (Humira) for Crohn's disease in pregnancy. Inflamm Bowel Dis 2006, 12:827-828.
80. Vesga L, Terdiman JP, Mahadevan U. Adalimumab use in pregnancy. Gut 2005, 54:890. 1774554, 15888806.
81. Organization of Teratology Information Specialists 2011, http://www.mothertobaby.org/about-s15418.
82. Gisbert JP. Safety of immunomodulators and biologics for the treatment of inflammatory bowel disease during pregnancy and breast-feeding. Inflamm Bowel Dis 2010, 16:881-895.
83. Osting VC, Carter JD. A safety assessment of tumor necrosis factor antagonists during pregnancy. Expert Opin Drug Saf 2010, 9:421-429.
84. Steinberg SA, Ulmann TA. Certolizumab treatment of linear IgA dermatosis in a pregnant Crohn's colitis patient: a case study and review of the literature. Gastroenterology 2010, 138:S-698.
85. Mahadevan U, Abreau MT. Certolizumab use in pregnancy: low levels detected in cord blood. Gastroenterology 2009, 136:A-146.
86. Oussalah A, Bigard MA, Peyrin-Biroulet L. Certolizumab use in pregnancy. Gut 2009, 58:608.
87. Mahadevan U, Wolf DC, Stach C, Kosutic G, Williams S, Terpstra I, Clowse M. Outcomes of pregnancy in subjects exposed to certolizumab pegol. Am J Gastroenterol 2012, 107:S621.
88. Colombel JF, Sandborn WJ, Reinisch W, Mantzaris GJ, Kornbluth A, Rachmilewitz D, Lichtiger S, D'Haens G, Diamond RH, Broussard DL, Tang KL, van der Woude CJ, Rutgeerts P. Infliximab, azathioprine, or combination therapy for Crohn's disease. N Engl J Med 2010, 362:1383-1395.
89. Panaccione R, Ghosh S, Middleton S, Velazquez JRM, Khalif I, Flint L, van Hoogstraten HJ, Zheng H, Danese S, Rutgeerts P. Infliximab, azathioproine, or infliximab + azathioprine for treatment of moderate to severe ulcerative colitis: the UC SUCCESS trial. Gastroenterology 2011, 140:S-134.
90. Rychly DJ, DiPiro JT. Infections associated with tumor necrosis factor-alpha antagonists. Pharmacotherapy 2005, 25:1181-1192.
91. Treacy G. Using an analogous monoclonal antibody to evaluate the reproductive and chronic toxicity potential for a humanized anti-TNFalpha monoclonal antibody. Hum Exp Toxicol 2000, 19:226-228.
92. Roux CH, Brocq O, Breuil V, Albert C, Euller-Ziegler L. Pregnancy in rheumatology patients exposed to anti-tumour necrosis factor (TNF)-alpha therapy. Rheumatology (Oxford) 2007, 46:695-698.
93. Marchioni RM, Blonski W, Lichtenstein GR. Anti-TNF inhibitor therapy and fetal risk: A systematic literature review. Gastroenterology 2012, 142:S-248.
94. Melmed GY. Vaccination strategies for patients with inflammatory bowel disease on immunomodulators and biologics. Inflamm Bowel Dis 2009, 15:1410-1416.