The relationship between the intensity of intra-amniotic inflammation and the presence and severity of acute histologic chorioamnionitis in preterm gestation

Journal of Maternal-Fetal and Neonatal Medicine

Volumn 28, Issue 13, 2015, Pages 1500-1509

  Kim, Sun Min ^a   Romero, Roberto ^b,c,d   Park, Jeong Woo ^a   Oh, Kyung Joon ^a   Jun, Jong Kwan ^a   Yoon, Bo Hyun ^a,b  

^a Seoul National University College of Medicine   (South Korea)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Amniotic fluid; matrix metalloproteinase 8; prematurity; preterm birth

Indexed keywords

NEUTROPHIL COLLAGENASE; MMP8 PROTEIN, HUMAN;

ACINETOBACTER BAUMANNII; ACUTE HISTOLOGIC CHORIOAMNIONITIS; ADULT; AMNIOCENTESIS; AMNION FLUID; ARTICLE; BACTERIUM ISOLATE; BURKHOLDERIA CEPACIA; CANDIDA; CHORIOAMNIONITIS; CONTROLLED STUDY; CORYNEBACTERIUM; DISEASE MARKER; DISEASE SEVERITY; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; FEMALE; FUNISITIS; GARDNERELLA VAGINALIS; GESTATIONAL AGE; HUMAN; INTRA AMNIOTIC INFLAMMATION; KLEBSIELLA PNEUMONIAE; LACTOBACILLUS; LEUKOCYTE COUNT; MAJOR CLINICAL STUDY; PREGNANCY COMPLICATION; PREMATURITY; PREVALENCE; PRIORITY JOURNAL; STAPHYLOCOCCUS; STREPTOCOCCUS; UREAPLASMA; UREAPLASMA HOMINIS; UREAPLASMA PARVUM; UREAPLASMA UREALYTICUM; ACUTE DISEASE; CHEMISTRY; INFLAMMATION; METABOLISM; NEWBORN; PATHOLOGY; PLACENTA; PREGNANCY; PREMATURE BIRTH; SEVERITY OF ILLNESS INDEX; STATISTICS AND NUMERICAL DATA; YOUNG ADULT;

ACUTE DISEASE; ADULT; AMNIOCENTESIS; AMNIOTIC FLUID; CHORIOAMNIONITIS; FEMALE; HUMANS; INFANT, NEWBORN; INFLAMMATION; MATRIX METALLOPROTEINASE 8; PLACENTA; PREGNANCY; PREMATURE BIRTH; PREVALENCE; SEVERITY OF ILLNESS INDEX; YOUNG ADULT;

EID: 84941249258     PISSN: 14767058     EISSN: 14764954     Source Type: Journal    
DOI: 10.3109/14767058.2014.961009     Document Type: Article

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133. Soto E, Espinoza J, Nien JK, et al. Human beta-defensin-2: a natural antimicrobial peptide present in amniotic fluid participates in the host response to microbial invasion of the amniotic cavity. J Matern Fetal Neonatal Med 2007;20:15-22.
134. Kusanovic JP, Romero R, Mazaki-Tovi S, et al. Resistin in amniotic fluid and its association with intra-amniotic infection and inflammation. J Matern Fetal Neonatal Med 2008;21:902-16.
135. Mazaki-Tovi S, Romero R, Kusanovic JP, et al. Visfatin/Pre-B cell colony-enhancing factor in amniotic fluid in normal pregnancy, spontaneous labor at term, preterm labor and prelabor rupture of membranes: an association with subclinical intrauterine infection in preterm parturition. J Perinat Med 2008;36:485-96.
136. Nhan-Chang CL, Romero R, Kusanovic JP, et al. A role for CXCL13 (BCA-1) in pregnancy and intra-amniotic infection/inflammation. J Matern Fetal Neonatal Med 2008;21:763-75.
137. Park CW, Lee SM, Park JS, et al. The antenatal identification of funisitis with a rapid MMP-8 bedside test. J Perinat Med 2008;36:497-502.
138. Romero R, Espinoza J, Rogers WT, et al. Proteomic analysis of amniotic fluid to identify women with preterm labor and intraamniotic inflammation/infection: the use of a novel computational method to analyze mass spectrometric profiling. J Matern Fetal Neonatal Med 2008;21:367-88.
139. Vaisbuch E, Romero R, Erez O, et al. Total hemoglobin concentration in amniotic fluid is increased in intraamniotic infection/inflammation. Am J Obstet Gynecol 2008;199:426.e1-7.
140. Kusanovic JP, Romero R, Jodicke C, et al. Amniotic fluid soluble human leukocyte antigen-G in term and preterm parturition, and intra-amniotic infection/inflammation. J Matern Fetal Neonatal Med 2009;22:1151-66.
141. Lee J, Oh KJ, Yang HJ, et al. The importance of intra-amniotic inflammation in the subsequent development of atypical chronic lung disease. J Matern Fetal Neonatal Med 2009;22:917-23.
142. Massaro G, Scaravilli G, Simeone S, et al. Interleukin-6 and Mycoplasma hominis as markers of preterm birth and related brain damage: our experience. J Matern Fetal Neonatal Med 2009;22:1063-67.
143. Snegovskikh VV, Schatz F, Arcuri F, et al. Intra-amniotic infection upregulates decidual cell vascular endothelial growth factor (VEGF) and neuropilin-1 and -2 expression: implications for infection-related preterm birth. Reprod Sci 2009;16:767-80.
144. Soto E, Romero R, Richani K, et al. Evidence for complement activation in the amniotic fluid of women with spontaneous preterm labor and intra-amniotic infection. J Matern Fetal Neonatal Med 2009;22:983-92.
145. Vaisbuch E, Romero R, Erez O, et al. Fragment Bb in amniotic fluid: evidence for complement activation by the alternative pathway in women with intra-amniotic infection/inflammation. J Matern Fetal Neonatal Med 2009;22:905-16.
146. Gavilanes AW, Strackx E, Kramer BW, et al. Chorioamnionitis induced by intraamniotic lipopolysaccharide resulted in an interval-dependent increase in central nervous system injury in the fetal sheep. Am J Obstet Gynecol 2009;200:437.e1-8.
147. Pacora P, Romero R, Chaiworapongsa T, et al. Amniotic fluid angiopoietin-2 in term and preterm parturition, and intra-amniotic infection/inflammation. J Perinat Med 2009;37:503-11.
148. Romero R, Mazaki-Tovi S, Vaisbuch E, et al. Metabolomics in premature labor: a novel approach to identify patients at risk for preterm delivery. J Matern Fetal Neonatal Med 2010;23:1344-59.
149. Cruciani L, Romero R, Vaisbuch E, et al. Pentraxin 3 in amniotic fluid: a novel association with intra-amniotic infection and inflammation. J Perinat Med 2010;38:161-71.
150. Vaisbuch E, Hassan SS, Mazaki-Tovi S, et al. Patients with an asymptomatic short cervix (
151. Kusanovic JP, Romero R, Chaiworapongsa T, et al. Amniotic fluid sTREM-1 in normal pregnancy, spontaneous parturition at term and preterm, and intra-amniotic infection/inflammation. J Matern Fetal Neonatal Med 2010;23:34-47.
152. Mazaki-Tovi S, Romero R, Vaisbuch E, et al. Adiponectin in amniotic fluid in normal pregnancy, spontaneous labor at term, and preterm labor: a novel association with intra-amniotic infection/inflammation. J Matern Fetal Neonatal Med 2010;23:120-30.
153. Balbin M, Fueyo A, Knauper V, et al. Collagenase 2 (MMP-8) expression in murine tissue-remodeling processes. Analysis of its potential role in postpartum involution of the uterus. J Biol Chem 1998;273:23959-68.
154. Angus SR, Segel SY, Hsu CD, et al. Amniotic fluid matrix metalloproteinase-8 indicates intra-amniotic infection. Am J Obstet Gynecol 2001;185:1232-38.
155. Park JS, Romero R, Yoon BH, et al. The relationship between amniotic fluid matrix metalloproteinase-8 and funisitis. Am J Obstet Gynecol 2001;185:1156-61.
156. Shim SS, Romero R, Jun JK, et al. C-reactive protein concentration in vaginal fluid as a marker for intra-amniotic inflammation/infection in preterm premature rupture of membranes. J Matern Fetal Neonatal Med 2005;18:417-22.
157. th percentile are a marker for subsequent preterm premature rupture of membranes. Am J Obstet Gynecol 2005;192:109-13.
158. Lee SE, Romero R, Park CW, et al. The frequency and significance of intraamniotic inflammation in patients with cervical insufficiency. Am J Obstet Gynecol 2008;198:633.
159. Lee SE, Park IS, Romero R, et al. Amniotic fluid prostaglandin F2 increases even in sterile amniotic fluid and is an independent predictor of impending delivery in preterm premature rupture of membranes. J Matern Fetal Neonatal Med 2009;22:880-86.
160. Oh KJ, Lee SE, Jung H, et al. Detection of ureaplasmas by the polymerase chain reaction in the amniotic fluid of patients with cervical insufficiency. J Perinat Med 2010;38:261-68.
161. Kim BJ, Romero R, Mi Lee S, et al. Clinical significance of oligohydramnios in patients with preterm labor and intact membranes. J Perinat Med 2011;39:131-6.
162. Lee J, Lee SM, Oh KJ, et al. Fragmented forms of insulin-like growth factor binding protein-1 in amniotic fluid of patients with preterm labor and intact membranes. Reprod Sci 2011;18:842-49.
163. Pacora P, Chaiworapongsa T, Maymon E, et al. Funisitis and chorionic vasculitis: the histological counterpart of the fetal inflammatory response syndrome. J Matern Fetal Neonatal Med 2002;11:18-25.
164. Yoon BH, Romero R, Park JS, et al. 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;183:1124-29.
165. Yoon BH, Romero R, Shim JY, et al. C-reactive protein in umbilical cord blood: a simple and widely available clinical method to assess the risk of amniotic fluid infection and funisitis. J Matern Fetal Neonatal Med 2003;14:85-90.
166. Blanc WA. Pathways of fetal and early neonatal infection. Viral placentitis, bacterial and fungal chorioamnionitis. J Pediatr 1961;59:473-96.
167. Maudsley RF, Brix GA, Hinton NA, et al. Placental inflammation and infection. A prospective bacteriologic and histologic study. Am J Obstet Gynecol 1966;95:648-59.
168. Hillier SL, Witkin SS, Krohn MA, et al. The relationship of amniotic fluid cytokines and preterm delivery, amniotic fluid infection, histologic chorioamnionitis, and chorioamnion infection. Obstet Gynecol 1993;81:941-48.
169. Yoon BH, Yang SH, Jun JK, et al. Maternal blood C-reactive protein, white blood cell count, and temperature in preterm labor: a comparison with amniotic fluid white blood cell count. Obstet Gynecol 1996;87:231-37.
170. Yoon BH, Romero R, Moon JB, et al. The frequency and clinical significance of intra-amniotic inflammation in patients with a positive cervical fetal fibronectin. Am J Obstet Gynecol 2001;185:1137-42.
171. Lee SE, Romero R, Jung H, et al. 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 e291-6.
172. DiGiulio DB, Romero R, Amogan HP, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One 2008;3:e3056.
173. Chaiworapongsa T, Erez O, Kusanovic JP, et al. Amniotic fluid heat shock protein 70 concentration in histologic chorioamnionitis, term and preterm parturition. J Matern Fetal Neonatal Med 2008;21:449-61.
174. Erez O, Romero R, Tarca AL, et al. Differential expression pattern of genes encoding for anti-microbial peptides in the fetal membranes of patients with spontaneous preterm labor and intact membranes and those with preterm prelabor rupture of the membranes. J Matern Fetal Neonatal Med 2009;22:1103-15.
175. Romero R, Sepulveda W, Kenney JS, et al. Interleukin 6 determination in the detection of microbial invasion of the amniotic cavity. Ciba Found Symp 1992;167:205-20 (discussion 220-203).
176. Romero R, Yoon BH, Mazor M, et al. A comparative study of the diagnostic performance of amniotic fluid glucose, white blood cell count, interleukin-6, and gram stain in the detection of microbial invasion in patients with preterm premature rupture of membranes. Am J Obstet Gynecol 1993;169:839-51.
177. Allbert JR, Naef III RW, Perry Jr KG, et al. Amniotic fluid interleukin-6 and interleukin-8 levels predict the success of tocolysis in patients with preterm labor. J Soc Gynecol Investig 1994;1:264-8.
178. Stallmach T, Hebisch G, Joller H, et al. Expression pattern of cytokines in the different compartments of the feto-maternal unit under various conditions. Reprod Fertil Dev 1995;7:1573-80.
179. Arntzen KJ, Kjollesdal AM, Halgunset J, et al. TNF, IL-1, IL-6, IL-8 and soluble TNF receptors in relation to chorioamnionitis and premature labor. J Perinat Med 1998;26:17-26.
180. Hsu CD, Meaddough E, Aversa K, et al. Elevated amniotic fluid levels of leukemia inhibitory factor, interleukin 6, and interleukin 8 in intra-amniotic infection. Am J Obstet Gynecol 1998;179:1267-70.
181. Rogers BB, Alexander JM, Head J, et al. Umbilical vein interleukin-6 levels correlate with the severity of placental inflammation and gestational age. Hum Pathol 2002;33:335-40.
182. Mazzucchelli I, Avanzini MA, Ciardelli L, et al. Human amniotic fluid cells are able to produce IL-6 and IL-8. Am J Reprod Immunol 2004;51:198-203.
183. Holst RM, Mattsby-Baltzer I, Wennerholm UB, et al. Interleukin-6 and interleukin-8 in cervical fluid in a population of Swedish women in preterm labor: relationship to microbial invasion of the amniotic fluid, intra-amniotic inflammation, and preterm delivery. Acta Obstet Gynecol Scand 2005;84:551-57.
184. Jacobsson B, Mattsby-Baltzer I, Hagberg H. Interleukin-6 and interleukin-8 in cervical and amniotic fluid: relationship to microbial invasion of the chorioamniotic membranes. BJOG 2005;112:719-24.
185. Holst RM, Laurini R, Jacobsson B, et al. Expression of cytokines and chemokines in cervical and amniotic fluid: relationship to histological chorioamnionitis. J Matern Fetal Neonatal Med 2007;20:885-93.
186. Bryant-Greenwood GD, Yamamoto SY, Sadowsky DW, et al. Relaxin stimulates interleukin-6 and interleukin-8 secretion from the extraplacental chorionic cytotrophoblast. Placenta 2009;30:599-606.
187. Bamberg C, Fotopoulou C, Linder M, et al. Mid-trimester amniotic fluid concentrations of the proinflammatory cytokines IL-6, IL-8, TNF-alpha, and lipopolysaccharide binding protein in normal pregnancies: a prospective evaluation according to parity, gestational age, and fetal gender. J Perinat Med 2011;39:403-9.
188. Ogge G, Romero R, Lee DC, et al. Chronic chorioamnionitis displays distinct alterations of the amniotic fluid proteome. J Pathol 2011;223:553-65.
189. Park JC, Kim DJ, Kwak-Kim J. Upregulated amniotic fluid cytokines and chemokines in emergency cerclage with protruding membranes. Am J Reprod Immunol 2011;66:310-19.
190. Yoneda S, Shiozaki A, Yoneda N, et al. Prediction of exact delivery time in patients with preterm labor and intact membranes at admission by amniotic fluid interleukin-8 level and preterm labor index. J Obstet Gynaecol Res 2011;37:861-66.
191. Marconi C, de Andrade Ramos BR, Peracoli JC, et al. Amniotic fluid interleukin-1 beta and interleukin-6, but not interleukin-8 correlate with microbial invasion of the amniotic cavity in preterm labor. Am J Reprod Immunol 2011;65:549-56.
192. Romero R, Kadar N, Miranda J, et al. The diagnostic performance of the Mass Restricted (MR) score in the identification of microbial invasion of the amniotic cavity or intra-amniotic inflammation is not superior to amniotic fluid interleukin-6. J Matern Fetal Neonatal Med 2014;27:757-69.
193. Romero R, Miranda J, Chaiworapongsa T, et al. Prevalence and clinical significance of sterile intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Reprod Immunol 2014. [Epub ahead of print].
194. Hsu CD, Meaddough E, Aversa K, et al. The role of amniotic fluid L-selectin, GRO-alpha, and interleukin-8 in the pathogenesis of intraamniotic infection. Am J Obstet Gynecol 1998;178:428-32.
195. Yamada T, Matsubara S, Minakami H, et al. Chemotactic activity for polymorphonuclear leukocytes: meconium versus meconiumstained amniotic fluid. Am J Reprod Immunol 2000;44:275-78.
196. Yamada T, Minakami H, Matsubara S, et al. Meconium-stained amniotic fluid exhibits chemotactic activity for polymorphonuclear leukocytes in vitro. J Reprod Immunol 2000;46:21-30.
197. Kim SM, Romero R, Lee J, et al. The frequency and clinical significance of intra-amniotic inflammation in women with preterm uterine contractility but without cervical change: do the diagnostic criteria for preterm labor need to be changed? J Matern Fetal Neonatal Med 2012;25:1212-21.
198. Yoon BH, Jun JK, Romero R, et al. Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1beta, and tumor necrosis factor-alpha), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol 1997;177:19-26.
199. Keelan JA, Wang K, Chaiworapongsa T, et al. Macrophage inhibitory cytokine 1 in fetal membranes and amniotic fluid from pregnancies with and without preterm labour and premature rupture of membranes. Mol Hum Reprod 2003;9:535-40.
200. Chaiworapongsa T, Romero R, Tolosa JE, et al. Elevated monocyte chemotactic protein-1 in amniotic fluid is a risk factor for pregnancy loss. J Matern Fetal Neonatal Med 2002;12:159-64.
201. Jacobsson B, Holst RM, Wennerholm UB, et al. Monocyte chemotactic protein-1 in cervical and amniotic fluid: relationship to microbial invasion of the amniotic cavity, intra-amniotic inflammation, and preterm delivery. Am J Obstet Gynecol 2003;189:1161-67.
202. Esplin MS, Romero R, Chaiworapongsa T, et al. Amniotic fluid levels of immunoreactive monocyte chemotactic protein-1 increase during term parturition. J Matern Fetal Neonatal Med 2003;14:51-6.
203. Esplin MS, Romero R, Chaiworapongsa T, et al. Monocyte chemotactic protein-1 is increased in the amniotic fluid of women who deliver preterm in the presence or absence of intra-amniotic infection. J Matern Fetal Neonatal Med 2005;17:365-73.
204. Miller JD, Benjamin JT, Kelly DR, et al. Chorioamnionitis stimulates angiogenesis in saccular stage fetal lungs via CC chemokines. Am J Physiol Lung Cell Mol Physiol 2010;298:L637-45.
205. Jacobsson B, Holst RM, Andersson B, et al. Monocyte chemotactic protein-2 and -3 in amniotic fluid: relationship to microbial invasion of the amniotic cavity, intra-amniotic inflammation and preterm delivery. Acta Obstet Gynecol Scand 2005;84:566-71.
206. Romero R, Gomez R, Galasso M, et al. Macrophage inflammatory protein-1 alpha in term and preterm parturition: effect of microbial invasion of the amniotic cavity. Am J Reprod Immunol 1994;32:108-13.
207. Dudley DJ, Hunter C, Mitchell MD, et al. Elevations of amniotic fluid macrophage inflammatory protein-1 alpha concentrations in women during term and preterm labor. Obstet Gynecol 1996;87:94-8.
208. Mittal P, Romero R, Kusanovic JP, et al. CXCL6 (granulocyte chemotactic protein-2): a novel chemokine involved in the innate immune response of the amniotic cavity. Am J Reprod Immunol 2008;60:246-57.
209. Romero R, Espinoza J, Hassan S, et al. Soluble receptor for advanced glycation end products (sRAGE) and endogenous secretory RAGE (esRAGE) in amniotic fluid: modulation by infection and inflammation. J Perinat Med 2008;36:388-98.
210. Hamill N, Romero R, Gotsch F, et al. Exodus-1 (CCL20): evidence for the participation of this chemokine in spontaneous labor at term, preterm labor, and intrauterine infection. J Perinat Med 2008;36:217-27.
211. Keelan JA, Yang J, Romero RJ, et al. Epithelial cell-derived neutrophil-activating peptide-78 is present in fetal membranes and amniotic fluid at increased concentrations with intraamniotic infection and preterm delivery. Biol Reprod 2004;70:253-9.
212. Athayde N, Romero R, Maymon E, et al. A role for the novel cytokine RANTES in pregnancy and parturition. Am J Obstet Gynecol 1999;181:989-94.
213. Cohen J, Ghezzi F, Romero R, et al. GRO alpha in the fetomaternal and amniotic fluid compartments during pregnancy and parturition. Am J Reprod Immunol 1996;35:23-9.
214. Romero R, Ceska M, Avila C, et al. Neutrophil attractant/activating peptide-1/interleukin-8 in term and preterm parturition. Am J Obstet Gynecol 1991;165:813-20.
215. Bujold E, Romero R, Kusanovic JP, et al. Proteomic profiling of amniotic fluid in preterm labor using two-dimensional liquid separation and mass spectrometry. J Matern Fetal Neonatal Med 2008;21:697-713.
216. Cobo T, Palacio M, Navarro-Sastre A, et al. Predictive value of combined amniotic fluid proteomic biomarkers and interleukin-6 in preterm labor with intact membranes. Am J Obstet Gynecol 2009;200:499.e1-6.
217. Romero R, Kusanovic JP, Gotsch F, et al. Isobaric labeling and tandem mass spectrometry: a novel approach for profiling and quantifying proteins differentially expressed in amniotic fluid in preterm labor with and without intra-amniotic infection/inflammation. J Matern Fetal Neonatal Med 2010;23:261-80.
218. Hitti J, Lapidus JA, Lu X, et al. Noninvasive diagnosis of intraamniotic infection: proteomic biomarkers in vaginal fluid. Am J Obstet Gynecol 2010;203:32.e1-8.
219. Kashlan F, Smulian J, Shen-Schwarz S, et al. Umbilical vein interleukin 6 and tumor necrosis factor alpha plasma concentrations in the very preterm infant. Pediatr Infect Dis J 2000;19:238-43.
220. Naccasha N, Hinson R, Montag A, et al. Association between funisitis and elevated interleukin-6 in cord blood. Obstet Gynecol 2001;97:220-24.
221. Kim CJ, Yoon BH, Park SS, et al. Acute funisitis of preterm but not term placentas is associated with severe fetal inflammatory response. Hum Pathol 2001;32:623-29.
222. Wirbelauer J, Seidenspinner S, Thomas W, et al. Funisitis is associated with increased interleukin-10 gene expression in cord blood mononuclear cells in preterm infants 32 weeks of gestation. Eur J Obstet Gynecol Reprod Biol 2011;155:31-35.
223. Overbach AM, Daniel SJ, Cassady G. The value of umbilical cord histology in the management of potential perinatal infection. J Pediatr 1970;76:22-31.
224. Kim CJ, Yoon BH, Romero R, et al. Umbilical arteritis and phlebitis mark different stages of the fetal inflammatory response. Am J Obstet Gynecol 2001;185:496-500.
225. Goepfert AR, Andrews WW, Carlo W, et al. Umbilical cord plasma interleukin-6 concentrations in preterm infants and risk of neonatal morbidity. Am J Obstet Gynecol 2004;191:1375-81.