An elevated fetal interleukin-6 concentration can be observed in fetuses with anemia due to Rh alloimmunization: implications for the understanding of the fetal inflammatory response syndrome

References

• Gomez R, Romero R, Ghezzi F, Yoon BH, Mazor M, Berry SM. The fetal inflammatory response syndrome. Am J Obstet Gynecol 1998;179:194–202.
   PubMed Web of Science ®Google Scholar
• Gotsch F, Romero R, Kusanovic JP, Mazaki-Tovi S, Pineles BL, Erez O, Espinoza J, Hassan SS. The fetal inflammatory response syndrome. Clin Obstet Gynecol 2007;50:652–683.
   PubMed Web of Science ®Google Scholar
• American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference: definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit Care Med 1992;20:864–874.
   PubMed Web of Science ®Google Scholar
• Romero R, Gomez R, Ghezzi F, Yoon BH, Mazor M, Edwin SS, Berry SM. A fetal systemic inflammatory response is followed by the spontaneous onset of preterm parturition. Am J Obstet Gynecol 1998;179:186–193.
   PubMed Web of Science ®Google Scholar
• Yoon BH, Romero R, Park JS, Kim M, Oh SY, Kim CJ, Jun JK. The relationship among inflammatory lesions of the umbilical cord (funisitis), umbilical cord plasma interleukin 6 concentration, amniotic fluid infection, and neonatal sepsis. Am J Obstet Gynecol 2000;183:1124–1129.
   PubMed Web of Science ®Google Scholar
• Pacora P, Chaiworapongsa, T, Maymon E, Kim YM, Gomez R, Yoon BH, Ghezzi F, Berry SM, Qureshi F, Jacques SM, Funisitis and chorionic vasculitis: the histological counterpart of the fetal inflammatory response syndrome. J Matern Fetal Neonatal Med 2002;11:18–25.
   PubMedGoogle Scholar
• Berry SM, Romero R, Gomez R, Puder KS, Ghezzi F, Cotton DB, Bianchi DW. Premature parturition is characterized by in utero activation of the fetal immune system. Am J Obstet Gynecol 1995;173:1315–1320.
   PubMed Web of Science ®Google Scholar
• Gomez R, Ghezzi F, Romero R, Yoon BH, Mazor M, Berry SM. Two thirds of human fetuses with microbial invasion of the amniotic cavity have a detectable systemic cytokine response before birth. Am J Obstet Gynecol 1997;176:S14.
   Google Scholar
• Berry SM, Gomez R, Athayde N, Ghezzi F, Mazor M, Yoon BH, Edwin S, Romero R. The role of granulocyte colony stimulating factor in the neutrophilia observed in the fetal inflammatory response syndrome. Am J Obstet Gynecol 1998;178:S202.
   Google Scholar
• Romero R, Athayde N, Gomez R, Mazor M, Yoon BH, Edwin S, Ghezzi F, Berry SM. The fetal inflammatory response syndrome is characterized by the outpouring of a potent extracellular matrix degrading enzyme into the fetal circulation. Am J Obstet Gynecol 1998;178:S3.
   Google Scholar
• Romero R, Maymon E, Pacora P, Gomez R, Mazor M, Yoon BH, Berry SM. Further observations on the fetal inflammatory response syndrome: a potential homeostatic role for the soluble receptors of tumor necrosis factor alpha. Am J Obstet Gynecol 2000;183:1070–1077.
   PubMed Web of Science ®Google Scholar
• Romero R, Chaiworapongsa T, Espinoza J, Gomez R, Yoon BH, Edwin S, Mazor M, Maymon E, Berry S. Fetal plasma MMP-9 concentrations are elevated in preterm premature rupture of the membranes. Am J Obstet Gynecol 2002;187:1125–1130.
   PubMed Web of Science ®Google Scholar
• Espinoza J, Chaiworapongsa T, Romero R, Gomez R, Kim JC, Yoshimatsu J, Edwin S, Rathnasabapathy C, Yoon BH. Evidence of participation of soluble CD14 in the host response to microbial invasion of the amniotic cavity and intra-amniotic inflammation in term and preterm gestations. J Matern Fetal Neonatal Med 2002;12:304–312.
   PubMedGoogle Scholar
• Chaiworapongsa T, Romero R, Kim JC, Kim YM, Blackwell SC, Yoon BH, Gomez R. Evidence for fetal involvement in the pathologic process of clinical chorioamnionitis. Am J Obstet Gynecol 2002;186:1178–1182.
   PubMed Web of Science ®Google Scholar
• Lee SE, Romero R, Jung H, Park CW, Park JS, Yoon BH. The intensity of the fetal inflammatory response in intraamniotic inflammation with and without microbial invasion of the amniotic cavity. Am J Obstet Gynecol 2007;197:294–296.
   PubMed Web of Science ®Google Scholar
• Kim SK, Romero R, Chaiworapongsa T, Kusanovic JP, Mazaki-Tovi S, Mittal P, Erez O, Vaisbuch E, Gotsch F, Pacora P, Evidence of changes in the immunophenotype and metabolic characteristics (intracellular reactive oxygen radicals) of fetal, but not maternal, monocytes and granulocytes in the fetal inflammatory response syndrome. J Perinat Med 2009;37:543–552.
   PubMed Web of Science ®Google Scholar
• Mestan K, Yu Y, Thorsen P, Skogstrand K, Matoba N, Liu X, Kumar R, Hougaard DM, Gupta M, Pearson C, Cord blood biomarkers of the fetal inflammatory response. J Matern Fetal Neonatal Med 2009;22:379–387.
   PubMed Web of Science ®Google Scholar
• Cardenas I, Means RE, Aldo P, Koga K, Lang SM, Booth C, Manzur A, Oyarzun E, Romero R, Mor G. Viral infection of the placenta leads to fetal inflammation and sensitization to bacterial products predisposing to preterm labor. J Immunol 2010;185:1248–1257.
   PubMed Web of Science ®Google Scholar
• DiGiulio DB, Romero R, Kusanovic JP, Gomez R, Kim CJ, Seok KS, Gotsch F, Mazaki-Tovi S, Vaisbuch E, Sanders K, Prevalence and diversity of microbes in the amniotic fluid, the fetal inflammatory response, and pregnancy outcome in women with preterm pre-labor rupture of membranes. Am J Reprod Immunol 2010;64:38–57.
   PubMed Web of Science ®Google Scholar
• Madsen-Bouterse SA, Romero R, Tarca AL, Kusanovic JP, Espinoza J, Kim CJ, Kim JS, Edwin SS, Gomez R, Draghici S. The transcriptome of the fetal inflammatory response syndrome. Am J Reprod Immunol 2010;63:73–92.
   PubMed Web of Science ®Google Scholar
• Gomez R, Berry S, Yoon BH, Mazor M, Athayde N, Ghezzi F, Romero R. The hematologic profile of the fetus with systemic inflammatory response syndrome. Am J Obstet Gynecol 1998;178:S202.
   Google Scholar
• Yoon BH, Romero R, Jun JK, Maymon E, Gomez R, Mazor M, Park JS. An increase in fetal plasma cortisol but not dehydroepiandrosterone sulfate is followed by the onset of preterm labor in patients with preterm premature rupture of the membranes. Am J Obstet Gynecol 1998;179:1107–1114.
   PubMed Web of Science ®Google Scholar
• Romero R, Gomez R, Ghezzi F, Yoon BH, Mazor M, Berry SM, Silva M, Treadwell M, DeVore GR. A novel form of fetal cardiac dysfunction in preterm premature rupture of membranes. Am J Obstet Gynecol 1999;180:S27.
   Google Scholar
• Yanowitz TD, Jordan JA, Gilmour CH, Towbin R, Bowen A, Roberts JM, Brozanski BS. Hemodynamic disturbances in premature infants born after chorioamnionitis: association with cord blood cytokine concentrations. Pediatr Res 2002;51:310–316.
   PubMed Web of Science ®Google Scholar
• Romero R, Espinoza J, Goncalves LF, Gomez R, Medina L, Silva M, Chaiworapongsa, T, Yoon BH, Ghezzi F, Lee W, Fetal cardiac dysfunction in preterm premature rupture of membranes. J Matern Fetal Neonatal Med 2004;16:146–157.
   PubMedGoogle Scholar
• Yoon BH, Kim YA, Romero R, Kim JC, Park KH, Kim MH, Park JS. Association of oligohydramnios in women with preterm premature rupture of membranes with an inflammatory response in fetal, amniotic, and maternal compartments. Am J Obstet Gynecol 1999;181:784–788.
   PubMed Web of Science ®Google Scholar
• De FC, Toti P, Santopietro R, Stumpo M, Pecciarini L, Bagnoli F. Small thymus in very low birth weight infants born to mothers with subclinical chorioamnionitis. J Pediatr 1999;135:384–386.
   PubMed Web of Science ®Google Scholar
• Toti P, De Felice C, Stumpo M, Schurfeld K, Di LL, Vatti R, Bianciardi G, Buonocore G, Seemayer TA, Luzi P. Acute thymic involution in fetuses and neonates with chorioamnionitis. Hum Pathol 2000;31:1121–1128.
   PubMed Web of Science ®Google Scholar
• Di Naro E, Cromi A, Ghezzi F, Raio L, Uccella S, D'Addario V, Loverro G. Fetal thymic involution: a sonographic marker of the fetal inflammatory response syndrome. Am J Obstet Gynecol 2006;194:153–159.
   PubMed Web of Science ®Google Scholar
• Yinon Y, Zalel Y, Weisz B, Mazaki-Tovi S, Sivan E, Schiff E, Achiron R. Fetal thymus size as a predictor of chorioamnionitis in women with preterm premature rupture of membranes. Ultrasound Obstet Gynecol 2007;29:639–643.
   PubMed Web of Science ®Google Scholar
• Watterberg KL, Demers LM, Scott SM, Murphy S. Chorioamnionitis and early lung inflammation in infants in whom bronchopulmonary dysplasia develops. Pediatrics 1996;97:210–215.
   PubMed Web of Science ®Google Scholar
• Yoon BH, Romero R, Kim KS, Park JS, Ki SH, Kim BI, Jun JK. A systemic fetal inflammatory response and the development of bronchopulmonary dysplasia. Am J Obstet Gynecol 1999;181:773–779.
   PubMed Web of Science ®Google Scholar
• Yoon BH, Romero R, Shim JY, Lim JH, Choe G, Kadar N, Park M. ‘Atypical’ chronic lung disease of the newborn is linked to fetal systemic inflammation. Am J Obstet Gynecol 2002;187:S129.
   Google Scholar
• Yoon BH, Romero R, Yang SH, Jun JK, Kim IO, Choi JH, Syn HC. Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol 1996;174:1433–1440.
   PubMed Web of Science ®Google Scholar
• Yoon BH, Romero R, Park JS, Kim CJ, Kim SH, Choi JH, Han TR. Fetal exposure to an intra-amniotic inflammation and the development of cerebral palsy at the age of three years. Am J Obstet Gynecol 2000;182:675–681.
   PubMed Web of Science ®Google Scholar
• Bashiri A, Burstein E, Mazor M. Cerebral palsy and fetal inflammatory response syndrome: a review. J Perinat Med 2006;34:5–12.
   PubMed Web of Science ®Google Scholar
• Kim YM, Kim GJ, Kim MR, Chaiworapongsa T, Espinoza J, Yoon BH, Bujold E, Romero R. Skin: An active component of the fetal innate immune system. Am J Obstet Gynecol 2003;189:S74.
   Google Scholar
• Kim YM, Romero R, Chaiworapongsa T, Espinoza J, Mor G, Kim CJ. Dermatitis as a component of the fetal inflammatory response syndrome is associated with activation of Toll-like receptors in epidermal keratinocytes. Histopathology 2006;49:506–514.
   PubMed Web of Science ®Google Scholar
• Moise KJ Jr. Management of rhesus alloimmunization in pregnancy. Obstet Gynecol 2008;112:164–176.
   PubMed Web of Science ®Google Scholar
• Radunovic N, Lockwood CJ, Alvarez M, Plecas D, Chitkara U, Berkowitz RL. The severely anemic and hydropic isoimmune fetus: changes in fetal hematocrit associated with intrauterine death. Obstet Gynecol 1992;79:390–393.
   PubMed Web of Science ®Google Scholar
• van Kamp IL, Klumper FJ, Bakkum RS, Oepkes D, Meerman RH, Scherjon SA, Kanhai HH. The severity of immune fetal hydrops is predictive of fetal outcome after intrauterine treatment. Am J Obstet Gynecol 2001;185:668–673.
   PubMed Web of Science ®Google Scholar
• Liley AW. Liquor amnil analysis in the management of the pregnancy complicated by resus sensitization. Am J Obstet Gynecol 1961;82:1359–70.
   PubMed Web of Science ®Google Scholar
• Mari G, Deter RL, Carpenter RL, Rahman F, Zimmerman R, Moise KJ Jr, Dorman KF, Ludomirsky A, Gonzalez R, Gomez R, Noninvasive diagnosis by Doppler ultrasonography of fetal anemia due to maternal red-cell alloimmunization. Collaborative Group for Doppler assessment of the blood velocity in anemic fetuses. N Engl J Med 2000;342:9–14.
   PubMed Web of Science ®Google Scholar
• Yoon BH, Romero R, Moon JB, Shim SS, Kim M, Kim G, Jun JK. Clinical significance of intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2001;185:1130–1136.
   PubMed Web of Science ®Google Scholar
• Ghezzi F, Romero R, Maymon E, Redman M, Blackwell S, Berry S M Fetal blood sampling. Fleischer A, Manning F, Jeanty P, Romero R (eds). Sonography in Obstetrics and Gynecology: Principles and Practice, 6th Edition. New York: McGraw-Hill, 2001;775–804.
   Google Scholar
• Nicolaides KH, Rodeck CH, Millar DS, Mibashan RS. Fetal haematology in rhesus isoimmunisation. Br Med J (Clin Res Ed) 1985;290:661–663.
   PubMed Web of Science ®Google Scholar
• Moise KJ Jr. Management of rhesus alloimmunization in pregnancy. Obstet Gynecol 2002;100:600–611.
   PubMed Web of Science ®Google Scholar
• Regulation of the acute phase and immune responses: interleukin-6. Ann NY Acad Sci 1989;557:1–583.
   PubMed Web of Science ®Google Scholar
• Jones SA. Directing transition from innate to acquired immunity: defining a role for IL-6. J Immunol 2005;175:3463–3468.
   PubMed Web of Science ®Google Scholar
• Akira S, Hirano T, Taga T, Kishimoto T. Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF). FASEB J 1990;4:2860–2867.
   PubMed Web of Science ®Google Scholar
• Hirano T, Akira S, Taga T, Kishimoto T. Biological and clinical aspects of interleukin 6. Immunol Today 1990; 11:443–449.
   PubMedGoogle Scholar
• Kishimoto T, Hibi M, Murakami M, Narazaki M, Saito M, Taga T. The molecular biology of interleukin 6 and its receptor. Ciba Found Symp 1992;167:5–16; discussion 16–23.
   PubMedGoogle Scholar
• Raj DS. Role of interleukin-6 in the anemia of chronic disease. Semin Arthritis Rheum 2009;38:382–388.
   PubMed Web of Science ®Google Scholar