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Fetal-Placental Inflammation, but Not Adrenal Activation, Is Associated

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Fetal-Placental Inflammation, but Not Adrenal Activation, Is Associated Research www.AJOG.org OBSTETRICS Fetal-placental inflammation, but not adrenal activation, is associated with extreme preterm delivery Sunita Trivedi, MD; Maria Joachim, BS; Thomas McElrath, MD, PhD; Harvey J. Kliman, MD, PhD; Elizabeth N. Allred, MS; Raina N. Fichorova, MD, PhD; Andrew Onderdonk, PhD; Fernanda Heitor, MD; Leila Chaychi, MD; Alan Leviton, MD; Joseph A. Majzoub, MD; for the Extremely Low Gestational Age Newborns (ELGAN) study investigators OBJECTIVE: Spontaneous labor at term involves the activation of pla- RESULTS: Among infants delivered at less than 28 weeks’ gestation, cental corticotropin-releasing hormone and the fetal adrenal axis, but spontaneous (vs induced) delivery was associated with less placental the basis for extreme preterm labor is unknown. Our objective was to corticotropin-releasing hormone expression and more frequent signs of determine whether placental corticotropin-releasing hormone is acti- placental inflammation and infection. vated in extreme preterm labor. STUDY DESIGN: One thousand five hundred six mothers delivering at less CONCLUSION: Inflammation and infection, rather than premature acti- than 28 weeks’ gestation were enrolled. Each mother/infant pair was as- vation of the fetal adrenal axis, should be the major focus of research to signed to the category that described the primary reason for hospitalization. prevent extremely preterm human birth. Observers who had no knowledge of patient categorization assessed pla- centa microbiology, histology, and corticotropin-releasing hormone expres- Key words: corticotropin-releasing hormone, infection, inflammation, sion. These were correlated with the primary reason for hospitalization. preterm delivery Cite this article as: Trivedi S, Joachim M, McElrath T, et al. Fetal-placental inflammation, but not adrenal activation, is associated with extreme preterm delivery. Am J Obstet Gynecol 2012;206:236.e1-8. n normal parturition, prostaglandins livery likely differ in ways that should guide risk of neurologic disorders in ELGANs.9 Iinitiate uterine contraction, aided by the development of better diagnostic and During the years 2002-2004, women deliv- a fall in progesterone’s effect to maintain therapeutic interventions.8 ering between a gestation of 22 weeks 0 uterine quiescence.1,2 As in other mam- days and 27 weeks 6 days at 1 of 14 partic- mals, activation of the human fetal adre- ipating institutions in 11 cities in 5 states nal axis plays an important role in normal MATERIALS AND METHODS were asked to enroll in the study. The indi- term parturition, with anthropoid pri- Study population vidual institutional review boards ap- mates uniquely using placental corticotro- The Extremely Low Gestational Age New- proved the enrollment and consent pro- pin-releasing hormone (CRH) to drive borns (ELGAN) study was designed to cesses. Mothers were approached for this process.3-7 However, the mechanisms identify pregnancy and neonatal charac- consent either upon antenatal admission that lead to normal and very preterm de- teristics and exposures that increase the or shortly after delivery, depending on clinical circumstance and institutional preference. From the Division of Endocrinology, Department of Medicine (Drs Trivedi, Heitor, Chaychi, and Of 1506 infants enrolled in the ELGAN Majzoub and Ms Joachim), and the Neuroepidemiology Unit, Department of Neurology (Ms Allred study, placentas were collected from and Dr Leviton), Children’s Hospital Boston; the Division of Maternal–Fetal Medicine (Dr Elrath) and 1411, ribonucleic acid (RNA) was pre- the Laboratory of Genital Tract Biology (Dr Fichorova), Department of Obstetrics, Gynecology, and Reproductive Biology, and the Clinical Microbiology Laboratory, Department of Pathology (Dr pared from 1370, and 1219 contained Onderdonk), Brigham and Women’s Hospital, Harvard Medical School, Boston, MA; and the nondegraded RNA. These 1219 placen- Department of Obstetrics, Gynecology and Reproductive Sciences, Yale University School of tas constitute the sample for all the ta- Medicine, New Haven, CT (Dr Kliman). bles. The 3 samples (1506, 1411, and Received Sept. 19, 2011; revised Nov. 12, 2011; accepted Dec. 9, 2011. 1219) are comparable in their propor- This study was supported by a cooperative agreement with the National Institute of Neurological tion of children delivered for maternal Disorders and Stroke (5U01NS040069-05), by a center grant award from the National Institute of and fetal reasons and the distribution of Child Health and Human Development (NIH-P30-HD-18655), and by the Timothy Murphy Fund. gestational ages and birthweights. The authors report no conflict of interest. The first 2 authors contributed equally. Pregnancy variables Reprints: Joseph A. Majzoub, MD, Division of Endocrinology, Department of Medicine, Children’s The clinical circumstances that led to Hospital Boston, Harvard Medical School, 300 Longwood Ave., Boston, MA 02115. [email protected]. preterm delivery were operationally de- 0002-9378/$36.00 • © 2012 Published by Mosby, Inc. • doi: 10.1016/j.ajog.2011.12.004 fined using both data from the maternal interview and data abstracted from the 236.e1 American Journal of Obstetrics & Gynecology MARCH 2012 www.AJOG.org Obstetrics Research diagnosis of preterm premature rupture FIGURE 1 of fetal membranes (pPROM) was de- Placental CRH mRNA (qRT-PCR), gestational ages 23-27 weeks fined as the presence of vaginal pooling with either documented nitrazine posi- tive testing or ferning prior to regular uterine activity. Preeclampsia was de- fined as new-onset hypertension and proteinuria of sufficient severity to war- rant delivery for either a maternal or fetal indication. For a diagnosis of cervical insuffi- ciency, a woman had to present with cer- vical dilation of greater than 2 cm, in the absence of membrane rupture and de- tected or perceived uterine activity. Pla- cental abruption was defined as presen- tation with significant amount of vaginal bleeding (either documented in the medical record or a postpartum hemat- ocrit Ͻ24%) and a clinical diagnosis of placental abruption in the absence of cervical change. Although painful uter- Abrupt, placental abruption (n ϭ 125); CI, cervical incompetence (n ϭ 74); CRH, corticotropin-releasing hormone; FI, fetal indication (n ϭ 62); PE, preeclampsia (n ϭ 163); pPROM, prelabor premature rupture of membranes (n ϭ 253); PTL, preterm labor (n ϭ 542); ine contractions were not required, most qRT-PCR, quantitative reverse transcription-polymerase chain reaction. women given this diagnosis tended to Trivedi. Fetal-placental inflammation, not adrenal activation, in extreme preterm delivery. Am J Obstet Gynecol 2012. present with vaginal hemorrhage often accompanied or very soon followed by labor. medical record.10 Each mother/infant ization: preterm labor was defined as In addition, placenta abruption, as de- pair was assigned to the category that de- progressive cervical dilation with regular fined, tended to be much more like the scribed the primary reason for hospital- contractions and intact membranes. The other spontaneous disorders of labor, prelabor rupture of membranes, and 10,11 FIGURE 2 cervical insufficiency. Presentations Placental CRH mRNA (RNA blot), gestational ages 23-27 weeks under the category of fetal indication/in- trauterine growth restriction included severe intrauterine growth restriction based on antepartum ultrasound exami- nation, nonreassuring fetal testing, oli- gohydramnious, and Doppler abnor- malities of umbilical cord blood flow. Preterm labor, prelabor premature rup- ture of fetal membranes, cervical insuffi- ciency, and placental abruption were then grouped into spontaneous deliveries be- cause they were initiated without medical assistance. “Induced for maternal or fetal reasons” is applied to deliveries that were not initiated by the mother or fetus but by the physician to preserve the health of mother or fetus. Placenta characteristics Delivered placentas were placed in a ster- ile examination basin and transported to Abrupt, placental abruption (n ϭ 96); CI, cervical incompetence (n ϭ 59); CRH, corticotropin-releasing hormone; FI, fetal indication (n ϭ 50); PE, preeclampsia (n ϭ 129); pPROM, prelabor premature rupture of membranes (n ϭ 206); PTL, preterm labor (n ϭ 415). a sampling room. Eighty-two percent of Trivedi. Fetal-placental inflammation, not adrenal activation, in extreme preterm delivery. Am J Obstet Gynecol 2012. the samples were obtained within 1 hour of delivery. MARCH 2012 American Journal of Obstetrics & Gynecology 236.e2 Research Obstetrics www.AJOG.org CRH messenger RNA content: RNA isola- tion. In placentas from which RNA was TABLE 1 prepared, CRH and ACTB mRNA (actin Percent of infants by delivery indication (column) B, a control messenger RNA [mRNA] and characteristic (row) ubiquitously expressed in all cells) ex- Delivery indication pression was analyzed by quantitative re- Row Characteristic PTL pPROM CI Abrupt FI PE number verse transcription-polymerase chain re- Antenatal steroid course action (PCR) and RNA blot. Biopsies of ..................................................................................................................................................................................................................................... Complete 55 73 78 62 66 67 771 the fetal side of the placenta to a depth of ....................................................................................................................................................................................................................................
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