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• W3157190149 abstract "See “Paternal exposure to immunosuppressive and/or biologic agents and birth outcomes in patients with immune-mediated inflammatory diseases,” by Meserve J, Luo J, Zhu W, et al, on page 107. See “Paternal exposure to immunosuppressive and/or biologic agents and birth outcomes in patients with immune-mediated inflammatory diseases,” by Meserve J, Luo J, Zhu W, et al, on page 107. There has been substantial research on maternal use of biologics and immunomodulators during pregnancy and short-term birth outcomes.1Broms G. Kieler H. Ekbom A. et al.Anti-TNF treatment during pregnancy and birth outcomes: a population-based study from Denmark, Finland and Sweden.Pharmacoepidemiol Drug Saf. 2020; 29: 316-327Crossref PubMed Scopus (16) Google Scholar, 2Luu M. Benzenine E. Doret M. et al.Continuous anti-TNF alpha use throughout pregnancy: possible complications for the mother but not for the fetus. A retrospective cohort on the French national health insurance database (EVASION).Am J Gastroenterol. 2018; 113: 1669-1677Crossref PubMed Scopus (81) Google Scholar, 3Kanis S.L. de Lima-Karagiannis A. de Boer N.K.H. et al.Use of thiopurines during conception and pregnancy is not associated with adverse pregnancy outcomes or health of infants at one year in a prospective study.Clin Gastroenterol Hepatol. 2017; 15: 1232-1241Abstract Full Text Full Text PDF PubMed Scopus (30) Google Scholar One presumed mechanism of a potential adverse impact of thiopurines on the fetus is a teratogenic effect. Fetal exposure to very high doses of thiopurines in animal studies has resulted in congenital abnormalities. Inflixmab, adalimumab, vedolizumab, and ustekinumab are actively transported across the placenta in the last 2 trimesters and might have potential adverse effects on the developing fetal immune system and organ development. There are in general few data on long-term health outcomes in the offspring after in utero medication exposure. Barker and Thornburg4Barker D.J. Thornburg K.L. The obstetric origins of health for a lifetime.Clin Obstet Gynecol. 2013; 56: 511-519Crossref PubMed Scopus (165) Google Scholar,5Barker D.J. The origins of the developmental origins theory.J Intern Med. 2007; 261: 412-417Crossref PubMed Scopus (1440) Google Scholar have suggested that several diseases of adult life originate from impaired intrauterine growth and development, and some follow-up studies have supported this hypothesis. Such chronic diseases in adulthood may thus be a consequence of “fetal programming,” whereby an insult such as a potentially harmful medical therapy at a critical, sensitive period of early life has permanent effects on structure, physiology, and metabolism. The PIANO study, the largest prospective study of pregnant women with inflammatory bowel disease published to date, demonstrated that treatment with biologics and immunomodulators during pregnancy was not associated with an increased risk of overall malformations, spontaneous abortions, preterm birth, low birthweight, and infections in the first year of life.6Mahadevan U. Long M.D. Kane S.V. et al.Pregnancy and neonatal outcomes after fetal exposure to biologics and thiopurines among women with inflammatory bowel disease.Gastroenterology. 2021; 160: 1131-1139Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar Population-based studies of in utero exposure to anti–tumor necrosis factor (TNF) and/or thiopurine medications and short-term birth outcomes have reported similarly reassuring results, although further research is still needed in this area.1Broms G. Kieler H. Ekbom A. et al.Anti-TNF treatment during pregnancy and birth outcomes: a population-based study from Denmark, Finland and Sweden.Pharmacoepidemiol Drug Saf. 2020; 29: 316-327Crossref PubMed Scopus (16) Google Scholar, 2Luu M. Benzenine E. Doret M. et al.Continuous anti-TNF alpha use throughout pregnancy: possible complications for the mother but not for the fetus. A retrospective cohort on the French national health insurance database (EVASION).Am J Gastroenterol. 2018; 113: 1669-1677Crossref PubMed Scopus (81) Google Scholar, 3Kanis S.L. de Lima-Karagiannis A. de Boer N.K.H. et al.Use of thiopurines during conception and pregnancy is not associated with adverse pregnancy outcomes or health of infants at one year in a prospective study.Clin Gastroenterol Hepatol. 2017; 15: 1232-1241Abstract Full Text Full Text PDF PubMed Scopus (30) Google Scholar Methodologically, pharmacoepidemiologic research has considerable requirements for the amount and quality of data, especially regarding assessment of rare short-term birth outcomes, and many studies are therefore limited in their ability to provide assurance of safety. This is especially true for studies of teratogenesis, as malformations cannot be regarded as a single homogeneous outcome, because exposure to a teratogen does not uniformly increase the rates of all malformations, but rather tends to increase the rates of selected malformations. Research on the associations between pregnant women with underlying diseases, medical treatments during pregnancy, and offspring outcomes is not complete without an analysis of a paternal impact. Recent animal and human studies have demonstrated that preconception paternal factors do affect the offspring. Paternal preconception stress, diet, and exposure to environmental toxins have been associated with altered hypothalamic-pituitary-adrenal axis function, birth defects, cancers, growth, obesity, and cardiometabolic risk factors in the offspring.7Braun J.M. Messerlian C. Hauser R. Fathers matter: why it's time to consider the impact of paternal environmental exposures on children's health.Curr Epidemiol Rep. 2017; 4: 46-55Crossref PubMed Google Scholar,8Fullston T. McPherson N.O. Owens J.A. et al.Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an obesogenic diet.Physiol Rep. 2015; 3e12336Crossref PubMed Scopus (71) Google Scholar Furthermore, animal studies have documented that epigenetic modifications encoded in sperm are heritable and influence offspring phenotypes.8Fullston T. McPherson N.O. Owens J.A. et al.Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an obesogenic diet.Physiol Rep. 2015; 3e12336Crossref PubMed Scopus (71) Google Scholar,9Soubry A. Hoyo C. Jirtle R.L. et al.A paternal environmental legacy: evidence for epigenetic inheritance through the male germ line.Bioessays. 2014; 36: 359-371Crossref PubMed Scopus (216) Google Scholar Chemical/environmental exposures may induce oxidative stress that results in mitochondrial or nuclear DNA damage or affect the sperm epigenome by altering DNA methyltransferase or histone deacetylase activity and thus interfering with hormonal regulation or sperm development.7Braun J.M. Messerlian C. Hauser R. Fathers matter: why it's time to consider the impact of paternal environmental exposures on children's health.Curr Epidemiol Rep. 2017; 4: 46-55Crossref PubMed Google Scholar, 8Fullston T. McPherson N.O. Owens J.A. et al.Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an obesogenic diet.Physiol Rep. 2015; 3e12336Crossref PubMed Scopus (71) Google Scholar, 9Soubry A. Hoyo C. Jirtle R.L. et al.A paternal environmental legacy: evidence for epigenetic inheritance through the male germ line.Bioessays. 2014; 36: 359-371Crossref PubMed Scopus (216) Google Scholar Thus, preconception toxigenic exposures could increase the risk of disease by epigenetic modifications in the germline, and expectant fathers’ use of medication before conception should be considered from this perspective (Figure 1). In addition, seminal plasma may affect offspring independently of sperm by directly stimulating the reproductive tract to produce embryotrophic cytokines and growth factors that protect embryos from cell stress and to suppress production of embryotoxic signals.10Robertson S.A. Seminal plasma and male factor signalling in the female reproductive tract.Cell Tissue Res. 2005; 322: 43-52Crossref PubMed Scopus (319) Google Scholar,11Bromfield J.J. Schjenken J.E. Chin P.Y. et al.Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring.Proc Natl Acad Sci U S A. 2014; 111: 2200-2205Crossref PubMed Scopus (225) Google Scholar External factors that disrupt seminal fluid signaling may alter the metabolic phenotype of the offspring. The newly understood importance of preconception paternal influence on the offspring has significant implications. Men with immune-mediated inflammatory diseases are subject to a variety of preconception factors that can potentially affect the health of their offspring, including the illness itself and/or medical therapies. There have been a number of nationwide studies from Denmark regarding the safety of paternal immunosuppressive medications on short-term birth outcomes.12Larsen M.D. Friedman S. Magnussen B. Nørgård B.M. Birth outcome of children fathered by men treated with systemic corticosteroids during the conception period - a cohort study based on nationwide data.Basic Clin Pharmacol Toxicol. 2018; 122: 133-138Crossref PubMed Scopus (4) Google Scholar, 13Winter R.W. Larsen M.D. Magnussen B. Friedman S. Kammerlander H. Nørgård B.M. Birth outcomes after preconception paternal exposure to methotrexate: a nationwide cohort study.Reprod Toxicol. 2017; 74: 219-223Crossref PubMed Scopus (12) Google Scholar, 14Nørgård B.M. Magnussen B. Larsen M.D. Friedman S. Reassuring results on birth outcomes in children fathered by men treated with azathioprine/6-mercaptopurine within three months before conception–a nationwide cohort study.Gut. 2017; 66: 1761-1766Crossref PubMed Scopus (25) Google Scholar, 15Larsen M.D. Friedman S. Magnussen B. Nørgård B.M. Birth outcomes in children fathered by men treated with anti-TNF-α agents before conception.Am J Gastroenterol. 2016; 111: 1608-1613Crossref PubMed Scopus (25) Google Scholar In these studies, paternal use of azathioprine/mercaptopurine, infliximab, adalimumab, corticosteroids and methotrexate prior to conception showed reassuring results. Also, Grosen et al16Grosen A. Bungum M. Hvas C.L. et al.Vedolizumab does not impair sperm DNA integrity in men with inflammatory bowel disease.Gastroenterology. 2019; 156: 2342-2344Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar, 17Grosen A. Bungum M. Christensen L.A. et al.Semen quality and sperm DNA integrity in patients with severe active inflammatory bowel disease and effects of tumour necrosis factor-alpha inhibitors.J Crohns Colitis. 2019; 13: 564-571Crossref PubMed Scopus (9) Google Scholar, 18Grosen A. Nersting J. Bungum M. et al.Sperm DNA integrity is unaffected by thiopurine treatment in men with inflammatory bowel disease.J Crohns Colitis. 2019; 13: 3-11Crossref PubMed Scopus (10) Google Scholar examined sperm integrity in men with inflammatory bowel disease via the Sperm Chromatin Structure Assay, one of the most sensitive methods for assessing sperm DNA integrity. They found that thiopurines do not increase sperm DNA fragmentation, that thioguanines are not incorporated into sperm DNA, and that infliximab, adalimumab, and vedolizumab do not significantly impair sperm DNA integrity. The study from Meserve et al19Meserve J. Luo J. Zhu W. et al.Paternal exposure to immunosuppressive and/or biologic agents and birth outcomes in patients with immune-mediated inflammatory diseases.Gastroenterology. 2021; 161: 107-115Abstract Full Text Full Text PDF Scopus (1) Google Scholar concurs with these former results, and Meserve et al19Meserve J. Luo J. Zhu W. et al.Paternal exposure to immunosuppressive and/or biologic agents and birth outcomes in patients with immune-mediated inflammatory diseases.Gastroenterology. 2021; 161: 107-115Abstract Full Text Full Text PDF Scopus (1) Google Scholar did not find an increased risk of preterm birth, or low birth weight infants of fathers who had taken thiopurines, methotrexate, or biologics within 3 months before conception. The authors used the OptumLabs database to identify 7453 expectant fathers with immune-mediated inflammatory diseases and compared fathers with and without medication use and birth outcomes. They report the first outcomes of paternal vedolizumab and ustekinumab use as well as additional data on the safety of paternal preconception use of methotrexate, thiopurines, and anti-TNF medications. Regarding major congenital malformations, we believe that the results should be interpreted with caution. The numbers of these outcomes are relatively low and the statistical precision of the risk estimates should be taken into consideration. In fact, the risk of malformations (based on adjusted analyses [model 2]), was risk ratio 1.4 (95% confidence interval [CI] 0.78–2.31) after thiopurines, 2.07 (95% CI 0.74–4.38) for non-TNF biologics, and 1.43 (95% CI 0.61–2.78) for combination therapies. Some of the limitations were lack of data on maternal drug exposure, and parental alcohol/smoking, and no possibility of performing stratified analyses according to type of paternal disease. Meserve et al19Meserve J. Luo J. Zhu W. et al.Paternal exposure to immunosuppressive and/or biologic agents and birth outcomes in patients with immune-mediated inflammatory diseases.Gastroenterology. 2021; 161: 107-115Abstract Full Text Full Text PDF Scopus (1) Google Scholar add important data regarding the effect of paternal immune-mediated inflammatory diseases and requisite immunosuppressive medications on the offspring. Studies like this one are especially important, because pharmaceutical companies normally do not include pregnant women and men attempting to conceive in clinical trials. There is a long way to go before we have achieved sufficient data on the impact of fathers’ use of medications around the time of conception and health outcomes in the offspring. The evidence on short-term child outcomes is emerging, but there is a large research gap concerning reproductive outcomes on the long-term health consequences of exposed children.20Nørgård B.M. Jølving L.R. Larsen M.D. Friedman S. Parental IBD and long-term health outcomes in the offspring.Inflamm Bowel Dis. 2019; 25: 1339-1348Crossref PubMed Scopus (7) Google Scholar We need long-term cohort studies to understand how parental disease affects offspring across their lifespan." @default.
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• W3157190149 title "Does Fatherhood Matter? Preconception Use of Biologics and Immunomodulators by Fathers With Immune-Mediated Diseases and Birth Outcomes of Their Offspring" @default.
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