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Association Between Maternal Inflammatory Bowel Disease And Journal of Perinatology (2014) 34, 435–440 © 2014 Nature America, Inc. All rights reserved 0743-8346/14 www.nature.com/jp ORIGINAL ARTICLE Association between maternal inflammatory bowel disease and adverse perinatal outcomes D Getahun1,2, MJ Fassett3, GF Longstreth1, C Koebnick1, AM Langer-Gould1, D Strickland1 and SJ Jacobsen1 OBJECTIVE: To examine whether inflammatory bowel disease (IBD) is associated with ischemic/inflammatory conditions during pregnancy. STUDY DESIGN: A retrospective cohort study using the 2000 to 2012 Kaiser Permanente Southern California maternally-linked medical records (n = 395 781). The two major subtypes of IBD, ulcerative colitis and Crohn’s diseases were studied. Adjusted odds ratios (ORs) were used to quantify the associations. RESULT: A pregnancy complicated by IBD was associated with increased incidence of small-for-gestational age birth (OR = 1.46, 95% confidence interval (CI) = 1.14 to 1.88), spontaneous preterm birth (OR = 1.32, 95% CI = 1.00 to 1.76) and preterm premature rupture of membranes (OR = 1.95, 95% CI = 1.26 to 3.02). Further stratifying by IBD subtypes, only ulcerative colitis was significantly associated with increased incidence of ischemic placental disease, spontaneous preterm birth and preterm premature rupture of membranes. CONCLUSION: The findings underscore the potential impact of maternal IBD on adverse perinatal outcomes. Clinicians should be aware that the association between IBD and adverse perinatal outcome varies by IBD subtypes. Journal of Perinatology (2014) 34, 435–440; doi:10.1038/jp.2014.41; published online 20 March 2014 INTRODUCTION liver; these complications of CD tend to be more common with 15,16 Inflammatory bowel disease (IBD) is a generic term that refers colon involvement. Prior studies have reported associations to serious, chronic inflammatory conditions of the intestinal tract between IBD and selected adverse outcomes. However, the including ulcerative colitis (UC) and Crohn’s disease (CD). Many association between IBD and ischemic and inflammatory condi- patients with IBD are between the ages of 15 to 30 years,1 thereby tions during pregnancy has received little attention. We assessed including women of childbearing age. In most industrialized whether IBD is associated with increased risk of ischemic and countries, the prevalence of IBD has been increasing over the inflammatory obstetrical conditions and whether the risk varies by last several decades.1,2 In the United States, the prevalence of UC IBD subtype. and CD is estimated to be as high as 238 and 201 per 100 000, respectively.2 The etiology and pathogenesis of UC and CD remain largely METHODS unknown. However, genetic, geographic, immunologic, infectious We conducted a retrospective cohort study to assess the risk of ischemic and dietary factors may have important roles.2–10 Another and inflammatory conditions at the maternal–fetal interface on the basis of potential risk factor is the use of oral contraceptives.11 Although their IBD status. Medical records of 395 781 women delivering in all Kaiser there is currently no cure for the disorder, with medical and Permanente Southern California (KPSC), a large integrated managed care organization, were used for this study. Information for this study was surgical therapies, most women with these conditions have extracted from the 2000 to 2012 matched perinatal records, which healthy pregnancies and deliver healthy babies. However, adverse matches birth certificate records for all KPSC births (Perinatal Services pregnancy outcomes, including preterm birth, low-birth-weight – System) to maternal records of hospitalization, outpatient physician birth and cesarean delivery have been linked to UC and CD.12 14 encounters and pharmacy dispensing records. The Perinatal Service Both UC and CD often begin with a relapsing-remitting course System records information on all births in all KPSC hospitals (more than that progresses at a variable rate, and they also have some 31 000 annually), including maternal sociodemographic and behavioral symptoms in common. Despite these general similarities, there are characteristics, pregnancy complications, labor and delivery as well as fetal and neonatal outcomes. The hospitalization and outpatient physician some important differences between the two IBD subtypes. fi Inflammation in UC is mucosal and limited to the large bowel, encounter records were reviewed to determine International Classi cation of Diseases-9-Clinical Modification (ICD-9-CM) codes for services through- whereas CD is typically transmural with skip lesions and can out KPSC. involve the small bowel, large bowel and occasionally the upper We obtained information on patient demographic and behavioral 1 gastrointestinal tract. Furthermore, they share nongastrointest- characteristics as well as medical and obstetric histories, infant outcomes inal manifestations including disorders of the eyes, skin, joints and and prescription medication dispensing history. Drugs assessed included 1Department of Research & Evaluation, Kaiser Permanente Southern California Medical Group, Pasadena, CA, USA; 2Department of Obstetrics and Gynecology, Rutgers-Robert Wood Johnson Medical School, New Brunswick, NJ, USA and 3Department of Maternal-Fetal Medicine, West Los Angeles Medical Center, Kaiser Permanente Southern California Medical Group, Pasadena, CA, USA. Correspondence: Dr D Getahun, Department of Research & Evaluation, Kaiser Permanente Southern California Medical Group, 100 S Los Robles Avenue, 2nd Floor, Pasadena, CA 91101, USA. E-mail: [email protected] This work was presented at the 30th Annual Meeting of the Society for Maternal-Fetal Medicine (SMFM), Chicago, IL, USA, on 5 February 2010. Received 3 October 2013; revised 23 January 2014; accepted 27 January 2014; published online 20 March 2014 Inflammatory bowel disease and perinatal outcomes D Getahun et al 436 anti-inflammatory medication commonly used for IBD (5-aminosalicylic analyses after stratifying the data by chronic hypertension status (yes/no). acid (5-ASA) and corticosteroids) and medications commonly used for We also carried out a − 2 log likelihood test from logistic regression to test maintenance of remission in quiescent IBD (azathioprine and 6-mercapto- the significance modifying effect of chronic hypertension on the purine) as a surrogate measure of disease severity. Assessment of IBD association. Finally, because patients with a more severe form of IBD are medication dispensing comprised the period from 3 months before more likely than patients with a less severe form of IBD to have used 5-ASA conception date until the birth of the child. For each medication used medications, steroids or to have undergone surgery and the intervention during the index pregnancy, we formed the following levels of factors: (i) may act as a confounder, we estimated the association between IBD and for 5-ASA (absence of IBD prescription drug, 5-ASA only, 5-ASA plus the adverse outcomes, stratified by the type of IBD drug prescriptions steroids, 5-ASA plus immunomodulators) and (ii) for steroids (absence of dispensed. IBD prescription drug, steroids only and steroids plus immunomodulators). All statistical analyses were performed using SAS version 9.2 (SAS For the purposes of this study, we defined ischemic placental diseases as Institute, Cary, NC, USA). The study was approved by the Institutional pregnancy complicated by any one or more of the following obstetrical Review Board of KPSC. disorders: preeclampsia (hypertensive disorder detected for the first time after 20 weeks’ gestation combined with proteinuria and/or edema; ICD-9- CM codes 642.4 and 642.5); small-for-gestational age (SGA, birth weight that is less than the 10th percentile for gestational age on the basis of the RESULTS 2000 to 2012 race/ethnicity- and sex-specific nomogram (that is, an The prevalence of IBD was 130/100 000 singleton pregnancies internal standard)); and placental abruption (premature separation of a during the study period. Differences in the prevalence were normally implanted placenta; ICD-9-CM code 762.1). The association between IBD and inflammatory perinatal conditions was observed between IBD subtypes, with the greatest prevalence assessed by evaluating its association with preterm premature rupture of being recorded for UC (100/100 000 singleton pregnancies). CD membranes (preterm PROM, ICD-9-CM codes 658.1x) and chorioamnionitis was the least frequent subtype with a prevalence of 30/100 000 (ICD-9-CM codes 762.7 and 658.4x). Although preterm birth is often singleton pregnancies. described as a multifactorial disease, approximately two-thirds of affected Women with IBD tended to be older than those without IBD individuals show some degree of inflammation.17 Therefore, we further (Table 1). Race/ethnicity varied between women with IBD and examined risk of preterm birth associated with IBD. Gestational age (23 to those without IBD; in particular, there were more whites and fewer 42 weeks) was largely on the basis of clinical estimates. In cases in which Hispanics, African-Americans and Asian/Pacific Islanders among o information on clinical estimate of gestational age was missing ( 3%), the women with IBD. Women with IBD also had more formal interval between the last normal menstrual period and the infant’s date of birth was used. As the data do not distinguish women who experienced education and a greater frequency of smoking. Only women with labor from those who did not, we considered labor to have been present IBD took 5-aminosalicylates,
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