medigraphic.com
Federación Mexicana de Ginecología y Obstetricia, A.C.

2022, Número 08

<< Anterior Siguiente >>

Ginecol Obstet Mex 2022; 90 (08)


Síndrome de respuesta inflamatoria fetal: fisiopatología, desenlaces y estudio ecográfico prenatal

Molina-Giraldo S, Franco TRV, Torres-Valencia N

Idioma: Español
Referencias bibliográficas: 103
Paginas: 664-681
Archivo PDF: 289.48 Kb.


RESUMEN

Objetivo: Ofrecer al lector información amplia y suficiente acerca de este síndrome, con hincapié en el reconocimiento del daño multiorgánico fetal, que permita darle herramientas para establecer el diagnóstico oportuno y disminuir la morbilidad y mortalidad fetal y neonatal.
Metodología: Estudio retrospectivo con base en la búsqueda en las bases de datos de PubMed, EBSCO y Ovid de 2016 a 2021 de artículos de revisión, investigaciones originales, guías de práctica clínica y protocolos. Además, artículos clásicos y los correspondientes a búsquedas manuales para lograr la contextualización de los puntos tratados.
Resultados: Cuando la infección llega al feto, se despliega una respuesta proinflamatoria con secreción de citocinas, que son la base para el diagnóstico de síndrome de respuesta inflamatoria fetal. Cuando esta respuesta a la infección es desregulada, termina por generar un daño multiorgánico que puede ser reconocido por medio de herramientas no invasivas, como el ultrasonido fetal avanzado. Este reconocimiento permite iniciar la atención oportuna a fin de reducir las tasas de morbilidad y mortalidad perinatal.
Conclusión: La infección microbiana de la cavidad amniótica y del feto, con la generación subsecuente del síndrome de respuesta inflamatoria fetal, se asocia con daño multiorgánico que puede reconocerse en el ultrasonido avanzado y lograr la atención óptima y mejores desenlaces perinatales.


REFERENCIAS (EN ESTE ARTÍCULO)

  1. Vogel JP, Chawanpaiboon S, Moller A-B, Watananirun K, etal. The global epidemiology of preterm birth. Best Practice& Research Clinical Obstetrics & Gynaecology 2018; 52:3-12. doi:10.1016/j.bpobgyn.2018.04.003

  2. WHO. Preterm birth 2018. https://www.who.int/newsroom/fact-sheets/detail/preterm-birth

  3. Gold enberg RL, Culhane JF, Iams JD, Romero R. Epidemiologyand causes of preterm birth. Lancet 2008; 371 (9606):75-84. doi:10.1016/S0140-6736(08)60074-4

  4. Ozalkaya E, Karatekin G, Topcuoğlu S, Gürsoy T, et al. Morbidityin preterm infants with fetal inflammatory responsesyndrome. Pediatrics International 2016; 58 (9): 850-4.doi:10.1111/ped.12895

  5. Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infectionand preterm delivery. New England J Medicine 2000;342 (20): 1500-7. doi:10.1056/NEJM200005183422007

  6. Park CW, Kim SM, Park JS, Jun JK, et al. Fetal, amnioticand maternal inflammatory responses in early stage ofascending intrauterine infection, inflammation restrictedto chorio-decidua, in preterm gestation. J Matern-FetalNeonatal Med 2014; 27 (1): 98-105. doi:10.3109/14767058.2013.806898

  7. Francis F, Bhat V, Mondal N, Adhisivam B, Jacob S, DorairajanG, et al. Fetal inflammatory response syndrome (FIRS)and outcome of preterm neonates -a prospective analyticalstudy. J Matern-Fetal Neonatal Med 2019; 32 (3): 488-92.doi: 10.1080/14767058.2017.1384458

  8. Oh J-W, Park C-W, Moon KC, Park JS, et al. The relationshipamong the progression of inflammation in umbilical cord,fetal inflammatory response, early-onset neonatal sepsis,and chorioamnionitis. PLoS One 2019; 14 (11): e0225328.doi:10.1371/journal.pone.0225328

  9. Jung E, Romero R, Yeo L, Diaz-Primera R, et al., editors.The fetal inflammatory response syndrome: the originsof a concept, pathophysiology, diagnosis, and obstetricalimplications. Seminars in Fetal and Neonatal Medicine2020: Elsevier. doi: 10.1016/j.siny.2020.101146

  10. Gómez R, Romero R, Ghezzi F, Yoon BH, et al. The fetal inflammatoryresponse syndrome. Am J Obstet Gynecol 1998;179 (1): 194-202. doi:10.1016/S0002-9378(98)70272-8

  11. Gotsch F, Romero R, Kusanovic JP, Mazaki-Tovi S, et al. Thefetal inflammatory response syndrome. Clin Obstet Gynecol2007; 50 (3): 652-83. doi: 10.1097/GRF.0b013e31811ebef6

  12. Combs CA, Garite TJ, Lapidus JA, Lapointe JP, et al. Detectionof microbial invasion of the amniotic cavity by analysisof cervicovaginal proteins in women with preterm laborand intact membranes. Am J Obstet Gynecol 2015; 212 (4):482. e1-. e12. doi: 10.1016/j.ajog.2015.02.007

  13. Arreaza-Graterol M, Rojas-Barrera JD, Molina-Giraldo S.Síndrome de respuesta Inflamatoria fetal (FIRS): adaptacióncardiovascular. Revista Colombiana de Obstetricia yGinecología 2011; 62 (1): 71-81.

  14. Kim CJ, Romero R, Chaemsaithong P, Kim J-S. Chronicinflammation of the placenta: definition, classification,pathogenesis, and clinical significance. Am J Obstet Gynecol2015; 213 (4): S53-S69. doi:10.1016/j.ajog.2015.08.041

  15. Arad I, Ergaz Z. The fetal inflammatory response syndromeand associated infant morbidity. Infection 2004; 4: 8.

  16. Romero R, Chaiworapongsa T, Espinoza J. Micronutrientsand intrauterine infection, preterm birth andthe fetal inflammatory response syndrome. J Nutrition2003;133(5):1668S-73S. doi:10.1093/jn/133.5.1668S

  17. Janeway CA, Travers P, Walport M, Schlomchik M. ImmunobiologyGarland Science Publishing. 2005.

  18. Luyt C-E, Combes A, Deback C, Aubriot-Lorton M-H, et al.Herpes simplex virus lung infection in patients undergoingprolonged mechanical ventilation. American journal ofrespiratory and critical care medicine. 2007;175(9):935-42.doi:10.1164/rccm.200609-1322OC

  19. Romero R, Sirtori M, Oyarzun E, Avila C, et al. Infection andlabor V. Prevalence, microbiology, and clinical significanceof intraamniotic infection in women with preterm laborand intact membranes. American journal of obstetricsand gynecology. 1989;161(3):817-24. doi:10.1016/0002-9378(89)90409-2

  20. Fidel Jr PL, Romero R, Maymon E, Hertelendy F. Bacteria‐inducedor bacterial product‐induced preterm parturition inmice and rabbits is preceded by a significant fall in serumprogesterone concentrations. J Maternal‐Fetal Medicine1998; 7 (5): 222-6. doi:10.3109/14767059809020447

  21. Schumann RR, Zweigner J. A novel acute-phase marker: lipopolysaccharidebinding protein (LBP). 1999. doi:10.1515/CCLM.1999.047

  22. Fenton MJ, Golenbock DT. LPS‐binding proteins and receptors.J Leukocyte Biol 1998; 64 (1):25-32. doi:10.1002/jlb.64.1.25

  23. Kunze M, Klar M, Morfeld CA, Thorns B, et al. Cytokinesin noninvasively obtained amniotic fluid as predictors offetal inflammatory response syndrome. American journalof obstetrics and gynecology. 2016;215(1):96. e1-. e8.doi:10.1016/j.ajog.2016.01.181

  24. Pacora P, Chaiworapongsa T, Maymon E, Kim Y, et al. Funisitisand chorionic vasculitis: the histological counterpartof the fetal inflammatory response syndrome. J Maternal-Fetal Neonatal Med 2002; 11 (1): 18-25. doi:10.1080/jmf.11.1.18.25

  25. Kim CJ, Romero R, Chaemsaithong P, Chaiyasit N, et al.Acute chorioamnionitis and funisitis: definition, pathologicfeatures, and clinical significance. American journalof obstetrics and gynecology. 2015;213(4):S29-S52.doi:10.1016/j.ajog.2015.08.040

  26. Vaisbuch E, Romero R, Gomez R, Kusanovic JP, et al. Anelevated fetal interleukin-6 concentration can be observedin fetuses with anemia due to Rh alloimmunization: implicationsfor the understanding of the fetal inflammatoryresponse syndrome. J Maternal-Fetal Neonatal Med 2011;24 (3): 391-6. doi:10.3109/14767058.2010.507294

  27. Takahashi N, Nagamatsu T, Fujii T, Takahashi K, et al. Extremelyhigh levels of multiple cytokines in the cord bloodof neonates born to mothers with systemic autoimmunediseases. Cytokine. 2020;127:154926. doi:10.1016/j.cyto.2019.154926

  28. Bytautiene E, Vedernikov YP, Saade GR, Romero R, etal. IgE-independent mast cell activation augments contractilityof nonpregnant and pregnant guinea pig myometrium.Int Arch Allergy Immunol 2008;147(2):140-6.doi:10.1159/000135701

  29. Romero R, Kusanovic JP, Muñoz H, Gomez R, et al.Allergy-induced preterm labor after the ingestion of shellfish.J Maternal-Fetal Neonatal Med 2010;23(4):351-9.doi:10.3109/14767050903177193

  30. Romero R, Kusanovic JP, Gomez R, Lamont R, et al.The clinical significance of eosinophils in the amnioticfluid in preterm labor. J Maternal-Fetal Neonatal Med2010;23(4):320-9. doi:10.3109/14767050903168465

  31. Musilova I, Bestvina T, Hudeckova M, Michalec I, et al.Vaginal fluid interleukin-6 concentrations as a point-of-caretest is of value in women with preterm prelabor ruptureof membranes. Am J Obstet Gynecol 2016; 215 (5): 619.e1-. e12. doi:10.1016/j.ajog.2016.07.001

  32. Meister B, Herold M, Mayr A, Widschwendter M, et al.Interleukin-3, interleukin-6, granulocyte-macrophagecolony-stimulating factor and erythropoietin cord bloodlevels of preterm and term neonates. Eur J Pediatrics 1993;152 (7): 569-73. doi:10.1007/BF01954082

  33. Chaemsaithong P, Romero R, Korzeniewski SJ, Martinez-Varea A, et al. A point of care test for interleukin-6 inamniotic fluid in preterm prelabor rupture of membranes:a step toward the early treatment of acute intra-amnioticinflammation/infection. J Maternal-fetal Neonat Med2016; 29 (3): 360-7. doi:10.3109/14767058.2015.1006621

  34. Yoon B, Romero R, Shim J-Y, Shim S-S, et al. C-reactiveprotein in umbilical cord blood: a simple and widely availableclinical method to assess the risk of amniotic fluidinfection and funisitis. J Maternal-Fetal Neonatal Med2003;14(2):85-90. doi:10.1080/jmf.14.2.85.90

  35. Romero R, Miranda J, Kusanovic JP, Chaiworapongsa T, etal. Clinical chorioamnionitis at term I: microbiology of theamniotic cavity using cultivation and molecular techniques.J Perinatal Medicine. 2015;43(1):19-36. doi:10.1515/jpm-2014-0249

  36. Tchirikov M, Schlabritz-Loutsevitch N, Maher J, BuchmannJ, et al. Mid-trimester preterm premature rupture ofmembranes (PPROM): etiology, diagnosis, classification,international recommendations of treatment optionsand outcome. J Perinatal Medicine 2018; 46 (5): 465-88.doi:10.1515/jpm-2017-0027

  37. Spinillo A, Iacobone AD, Calvino IG, Alberi I, et al. Therole of the placenta in feto-neonatal infections. EarlyHuman Development 2014; 90: S7-S9. doi:10.1016/S0378-3782(14)70003-9

  38. Romero R, Gomez R, Ghezzi F, Yoon BH, et al. A fetal systemicinflammatory response is followed by the spontaneousonset of preterm parturition. Am J Obstet Gynecol1998;179(1):186-93. doi:10.1016/S0002-9378(98)70271-6

  39. Gantert M, Been J, Gavilanes A, Garnier Y, et al. Chorioamnionitis:a multiorgan disease of the fetus? J Perinatol2010;30(1):S21-S30. doi:10.1038/jp.2010.96

  40. Al-Haddad BJ, Oler E, Armistead B, Elsayed NA, et al. Thefetal origins of mental illness. Am J Obstet Gynecol 2019;221 (6): 549-62. doi:10.1016/j.ajog.2019.06.013

  41. Gilles FH, Leviton A, Kerr CS. Endotoxin leucoencephalopathyin the telencephalon of the newborn kitten. JNeurol Sciences 1976; 27 (2): 183-91. doi:10.1016/0022-510X(76)90060-5

  42. Chau V, McFadden DE, Poskitt KJ, Miller SP. Chorioamnionitisin the pathogenesis of brain injury in preterm infants.Clinics in Perinatology 2014; 41 (1): 83-103. doi:10.1016/j.clp.2013.10.009

  43. Muraskas J, Kelly A, Nash M, Goodman J, Morrison J. Therole of fetal inflammatory response syndrome and fetalanemia in nonpreventable term neonatal encephalopathy.J Perinatol 2016; 36 (5): 362-5. doi:10.1038/jp.2015.214

  44. Nelson KB. Epidemiology of cerebral palsy. Adv Neurol.1978;19:421-35. PMID: 369329

  45. Hassell KJ, Ezzati M, Alonso-Alconada D, Hausenloy DJ, etal. New horizons for newborn brain protection: enhancingendogenous neuroprotection. Archives of Disease inChildhood-Fetal and Neonatal Edition. 2015;100(6):F541-F52. doi:10.1136/archdischild-2014-306284

  46. Leviton A. Preterm birth and cerebral palsy: is tumor necrosisfactor the missing link? Developmental Medicine & ChildNeurology. 1993;35(6):553-8. doi:10.1038/pr.2013.238

  47. Kuypers E, Ophelders D, Jellema RK, Kunzmann S, et al.White matter injury following fetal inflammatory responsesyndrome induced by chorioamnionitis and fetal sepsis:lessons from experimental ovine models. Early humandevelopment. 2012;88(12):931-6. doi:10.1016/j.earlhumdev.2012.09.011

  48. Romero-Guzman GJ, Lopez-Munoz F. Prevalence and riskfactors for periventricular leukomalacia in preterm infants.A systematic review. Revista de Neurología 2017; 65 (2):57-62. doi:10.33588/rn.6502.2017002

  49. Allred EN, Capone Jr A, Fraioli A, Dammann O, et al. Retinopathyof prematurity and brain damage in the very pretermnewborn. J Am Assoc Pediatr Ophthalmol Strabismus 2014;18 (3): 241-7. doi:10.1016/j.jaapos.2014.01.014

  50. Villamor-Martinez E, Cavallaro G, Raffaeli G, MohammedRahim OM, et al. Chorioamnionitis as a risk factor for retinopathyof prematurity: An updated systematic reviewand meta-analysis. PloS One 2018; 13 (10): e0205838.doi:10.1371/journal.pone.0205838

  51. Park YJ, Woo SJ, Kim YM, Hong S, et al. Immune and inflammatoryproteins in cord blood as predictive biomarkers ofretinopathy of prematurity in preterm infants. InvestigativeOphthalmology & Visual Science. 2019;60(12):3813-20.doi:10.1167/iovs.19-27258

  52. Matarazzo L, Nider S, Battelino S, Muzzi E, et al. Meningitisas a consequence of otitis media in a child referred fromthe newborn hearing screening programme: A missedopportunity. J Paediatrics Child Health 2018;54(7):810-2.doi:10.1111/jpc.13864

  53. Leung JC, Cifra CL, Agthe AG, Sun C-CJ, et al. Antenatalfactors modulate hearing screen failure risk in preterminfants. Archives of Disease in Childhood-Fetal and NeonatalEdition. 2016;101(1):56-61. doi:10.1136/archdischild-2014-307843

  54. De Felice C, Bagnoli F, Toti P, Musarò MA, et al. Transienthypothyroxinemia of prematurity and histological chorioamnionitis.2005. doi:10.1515/JPM.2005.091

  55. Reuss ML, Paneth N, Pinto-Martin JA, Lorenz JM, et al. Therelation of transient hypothyroxinemia in preterm infantsto neurologic development at two years of age. NEJM 1996;334 (13): 821-7. doi:10.1056/NEJM199603283341303

  56. Romero R, Espinoza J, Goncalves L, Gomez R, et al. Fetalcardiac dysfunction in preterm premature rupture ofmembranes. J Maternal-Fetal Neonatal Med 2004; 16 (3):146-57. doi:10.1080/14767050400009279

  57. Kumar A, Parrillo JE, Kumar A. Clinical review: myocardialdepression in sepsis and septic shock. Critical care.2002;6(6):1-9. doi:10.1186/cc1822

  58. Hernandez‐Andrade E, Figueroa‐Diesel H, Kottman C, IllanesS, et al. Gestational‐age‐adjusted reference values forthe modified myocardial performance index for evaluationof fetal left cardiac function. Ultrasound in Obstetrics andGynecology: J Ultrasound Obstet Gynecol 2007; 29 (3):321-5. doi:10.1002/uog.3947

  59. Yanowitz TD, Ann Jordan J, Gilmour CH, Towbin R, et al.Hemodynamic disturbances in premature infants born afterchorioamnionitis: association with cord blood cytokineconcentrations. Pediatric Research 2002; 51 (3): 310-6.doi:10.1203/00006450-200203000-00008

  60. Wolfberg AJ, Norwitz ER. Probing the fetal cardiac signalfor antecedents of brain injury. Clinics in perinatology.2009;36(3):673-84. doi:10.1016/j.clp.2009.06.006

  61. Garnier Y, Coumans AB, Jensen A, Hasaart TH, et al.Infection-related perinatal brain injury: the pathogenic roleof impaired fetal cardiovascular control. J Gynecol Invest2003; 10 (8): 450-9. doi:10.1016/s1071-5576(03)00150-3

  62. Mitchell T, MacDonald JW, Srinouanpranchanh S, BammlerTK, et al. Evidence of cardiac involvement in the fetalinflammatory response syndrome: disruption of genenetworks programming cardiac development in nonhumanprimates. American journal of obstetrics and gynecology.2018;218(4):438. e1-. e16. doi:10.1016/j.ajog.2018.01.009

  63. Carr H, Cnattingius S, Granath F, Ludvigsson JF, et al.Preterm birth and risk of heart failure up to earlyadulthood. JACC 2017; 69 (21): 2634-42. doi:10.1016/j.jacc.2017.03.572

  64. Nguyen MU, Wallace MJ, Pepe S, Menheniott TR, et al. Perinatalinflammation: a common factor in the early origins ofcardiovascular disease? Clinical Science. 2015;129(8):769-84. doi:10.1042/CS20150045

  65. Vandenbroucke L, Doyen M, Le Lous M, Beuchée A, et al.Chorioamnionitis following preterm premature ruptureof membranes and fetal heart rate variability. Plos one.2017;12(9):e0184924. doi:10.1371/journal.pone.0184924

  66. Ugwumadu A. Understanding cardiotocographic patternsassociated with intrapartum fetal hypoxia and neurologicinjury. Best practice & research Clinical obstetrics& gynaecology. 2013;27(4):509-36. doi:10.1016/j.bpobgyn.2013.04.002

  67. Cassell G, Crouse D, Canupp K, Waites K, et al. Associationof Ureaplasma urealyticum infection of the lower respiratorytract with chronic lung disease and death in very-lowbirth-weight infants. The Lancet. 1988;332(8605):240-5.doi:10.1016/s0140-6736(88)92536-6

  68. Yoon BH, Romero R, Jun JK, Park KH, et al. Amnioticfluid cytokines (interleukin-6, tumor necrosis factor-α,interleukin-1β, and interleukin-8) and the risk for thedevelopment of bronchopulmonary dysplasia. Americanjournal of obstetrics and gynecology. 1997;177(4):825-30.doi:10.1016/s0002-9378(97)70276-x

  69. Thomas W, Speer CP. Chorioamnionitis is essential in theevolution of bronchopulmonary dysplasia–the case infavour. Paediatric respiratory reviews. 2014;15(1):49-52.doi:10.1016/j.prrv.2013.09.004

  70. Moss TJ, Nitsos I, Ikegami M, Jobe AH, et al. Experimentalintrauterine Ureaplasma infection in sheep. Americanjournal of obstetrics and gynecology. 2005;192(4):1179-86.doi:10.1016/j.ajog.2004.11.063

  71. Villamor-Martinez E, Álvarez-Fuente M, Ghazi AM, DegraeuweP, et al. Association of chorioamnionitis withbronchopulmonary dysplasia among preterm infants: asystematic review, meta-analysis, and metaregression.JAMA network open. 2019;2(11):e1914611-e. doi:10.1001/jamanetworkopen.2019.14611

  72. Rubarth LB, Quinn J. Respiratory development andrespiratory distress syndrome. Neonatal Network.2015;34(4):231-8. doi:10.1891/0730-0832.34.4.231

  73. Mastrolia SA, Erez O, Loverro G, Di Naro E, et al. Ultrasonographicapproach to diagnosis of fetal inflammatoryresponse syndrome: a tool for at-risk fetuses? AmericanJ Obstet Gynecol 2016; 215 (1): 9-20. doi:10.1016/j.ajog.2016.01.164

  74. Sciaky‐Tamir Y, Hershkovitz R, Mazor M, Shelef I, et al.The use of imaging technology in the assessment ofthe fetal inflammatory response syndrome—imaging ofthe fetal thymus. Prenatal Diagnosis. 2015;35(5):413-9.doi:10.1002/pd.4560

  75. Musilova I, Hornychova H, Kostal M, Jacobsson B, et al.Ultrasound measurement of the transverse diameter of thefetal thymus in pregnancies complicated by the pretermprelabor rupture of membranes. J Clin Ultrasound 2013;41 (5): 283-9. doi:10.1002/jcu.22027

  76. Di Naro E, Cromi A, Ghezzi F, Raio L, et al. Fetal thymicinvolution: a sonographic marker of the fetal inflammatoryresponse syndrome. American journal of obstetricsand gynecology. 2006;194(1):153-9. doi:10.1016/j.ajog.2005.05.036

  77. Kuypers E, Wolfs TG, Collins JJ, Jellema RK, et al. Intraamnioticlipopolysaccharide exposure changes cell populationsand structure of the ovine fetal thymus. Reproductive sciences.2013;20(8):946-56. doi:10.1177/1933719112472742

  78. Haeryfar S, Berczi I. The thymus and the acute phaseresponse. Cellular and molecular biology (Noisy-le-Grand,France). 2001;47(1):145-56. PMID: 11292249

  79. Melville JM, Bischof RJ, Meeusen EN, Westover AJ, et al.Changes in fetal thymic immune cell populations in a sheepmodel of intrauterine inflammation. Reproductive sciences.2012;19(7):740-7. doi:10.1177/1933719111432873

  80. Musilova I, Kacerovsky M, Hornychova H, Kostal M, et al.Pulsation of the fetal splenic vein–a potential ultrasoundmarker of histological chorioamnionitis and funisitis inwomen with preterm prelabor rupture of membranes. Actaobstetricia et gynecologica scandinavica. 2012;91(9):1119-23. DOI 10.1111/j.1600-0412.2012.01450.x

  81. Yoon BH, Romero R, Jun JK, Maymon E, et al. An increase infetal plasma cortisol but not dehydroepiandrosterone sulfateis followed by the onset of preterm labor in patients withpreterm premature rupture of the membranes. Americanjournal of obstetrics and gynecology. 1998;179(5):1107-14.doi:10.1016/s0002-9378(98)70114-0

  82. Molina-Giraldo S, Franco-Torres RV, Pulido-Montaña FA,Hincapié-Porras CF, et al. Measurement of the Volume ofthe Fetal Adrenal Gland in Two Latin American MaternalFetal Medicine Units. Int J Clin Case Reports 2021; 163-79.

  83. Wolfs TG, Buurman WA, Zoer B, Moonen RM, DerikxJP, Thuijls G, et al. Endotoxin induced chorioamnionitisprevents intestinal development during gestation in fetalsheep. PloS one. 2009;4(6):e5837. doi:10.1371/journal.pone.0005837

  84. Okazaki K, Kondo M, Kato M, Kakinuma R, et al. Serum cytokineand chemokine profiles in neonates with meconiumaspiration syndrome. Pediatrics. 2008;121(4):e748-e53.doi:10.1542/peds.2007-1697

  85. Lee J, Romero R, Lee KA, Kim EN, et al. Meconium aspirationsyndrome: a role for fetal systemic inflammation. Americanjournal of obstetrics and gynecology. 2016;214(3):366. e1-.e9. doi:10.1016/j.ajog.2015.10.009

  86. Bieghs V, Vlassaks E, Custers A, Van Gorp PJ, et al. Chorioamnionitisinduced hepatic inflammation and disturbedlipid metabolism in fetal sheep. Pediatric research.2010;68(6):466-72. doi:10.1203/PDR.0b013e3181f70eeb

  87. Molina Giraldo S, Alfonso Ayala DA, Arreaza Graterol M,Perez Olivo JL, et al. Three‐dimensional Doppler ultrasonographyfor the assessment of fetal liver vascularization infetuses with intrauterine growth restriction. Int J GynecolObstetrics 2019; 144 (3): 260-4. doi:10.1002/ijgo.12715

  88. Lee SE, Romero R, Lee SM, Yoon BH. Amniotic fluid volumein intra-amniotic inflammation with and withoutculture-proven amniotic fluid infection in pretermpremature rupture of membranes. 2010. doi:10.1515/jpm.2009.123

  89. Azpurua H, Dulay AT, Buhimschi IA, Bahtiyar MO, et al. Fetalrenal artery impedance as assessed by Doppler ultrasoundin pregnancies complicated by intraamniotic inflammationand preterm birth. American journal of obstetrics andgynecology. 2009;200(2):203. e1-. e11. doi:10.1016/j.ajog.2008.11.001

  90. Galinsky R, Moss TJ, Gubhaju L, Hooper SB, et al. Effectof intra-amniotic lipopolysaccharide on nephron numberin preterm fetal sheep. Am J Physiology-Renal Physiology2011; 301 (2): F280-F5. doi:10.1152/ajprenal.00066.2011

  91. Romero R, Savasan ZA, Chaiworapongsa T, Berry SM, etal. Hematologic profile of the fetus with systemic inflammatoryresponse syndrome. J Perinat Med 2012; 40 (1):19-32. doi:10.1515/JPM.2011.100

  92. Berry SM, Romero R, Gomez R, Puder KS, et al. Prematureparturition is characterized by in utero activation of thefetal immune system. American journal of obstetrics andgynecology. 1995;173(4):1315-20. doi:10.1016/0002-

  93. 9378(95)91378-593. Abdel-Razeq SS, Buhimschi IA, Bahtiyar MO, Rosenberg VA,et al. Interpretation of amniotic fluid white blood cell countin “bloody tap” amniocenteses in women with symptomsof preterm labor. Obstetrics and gynecology. 2010;116(2 01):344. doi: 10.1097/AOG.0b013e3181e8fec6

  94. Ferber A, Minior VK, Bornstein E, Divon MY. Fetal “nonreassuringstatus” is associated with elevation of nucleatedred blood cell counts and interleukin-6. Americanjournal of obstetrics and gynecology. 2005;192(5):1427-9.doi:10.1016/j.ajog.2004.12.076

  95. Maier R, Günther A, Vogel M, Dudenhausen J, et al. Umbilicalvenous erythropoietin and umbilical arterial pH inrelation to morphologic placental abnormalities. Obstetricsand Gynecology 1994;84(1):81-7. PMID: 8008330

  96. Kim Y, Romero R, Chaiworapongsa T, Espinoza J, et al.Dermatitis as a component of the fetal inflammatory responsesyndrome is associated with activation of Toll‐likereceptors in epidermal keratinocytes. Histopathology.2006;49(5):506-14. doi:10.1111/j.1365-2559.2006.02542.x

  97. Collins JJ, Kallapur SG, Knox CL, Nitsos I, et al. Inflammationin fetal sheep from intra-amniotic injection ofUreaplasma parvum. Am J Physiology-Lung Cellular andMolecular Physiology 2010; 299 (6): L852-L60. doi:10.1152/ajplung.00183.2010

  98. Madsen‐Bouterse SA, Romero R, Tarca AL, Kusanovic JP, etal. The transcriptome of the fetal inflammatory responsesyndrome. Am J Reprod Immunol 2010; 63 (1): 73-92.doi:10.1111/j.1600-0897.2009.00791.x

  99. Tang Q, Zhang L, Li H, Shao Y. The fetal inflammationresponse syndrome and adverse neonatal outcomes: ameta-analysis. J Maternal-Fetal Neonatal Med 2021; 34(23): 3902-14. doi:10.1080/14767058.2019.1702942

  100. Ericson JE, Laughon MM. Chorioamnionitis: implications forthe neonate. Clinics in Perinatology 2015; 42 (1): 155-65.doi:10.1016/j.clp.2014.10.011

  101. Kacerovský M, Musilova I. Management of preterm prelaborrupture of membranes with respect to the inflammatorycomplications-our experiences. Ceska Gynekologie2013; 78 (6): 509-13. PMID: 24372427

  102. Kacerovsky M, Romero R, Stepan M, Stranik J, et al. Antibioticadministration reduces the rate of intraamnioticinflammation in preterm prelabor rupture of the membranes.Am J Obstet Gynecol 2020; 223 (1): 114. e1-. e20.doi: 10.1016/j.ajog.2020.01.043

  103. Johnson CT, Adami RR, Farzin A. Antibiotic therapy forchorioamnionitis to reduce the global burden of associateddisease. Frontiers in Pharmacology 2017; 8: 97. doi:10.3389/fphar.2017.00097




2020     |     www.medigraphic.com