CXCL10 and IL-6: Markers of two different forms of intra-amniotic inflammation in preterm labor

American Journal of Reproductive Immunology

Volumn 78, Issue 1, 2017, Pages

  Romero, Roberto ^a,b,c,d,e   Chaemsaithong, Piya ^a,b,e   Chaiyasit, Noppadol ^a,b,e   Docheva, Nikolina ^a,b,e   Dong, Zhong ^a,b,e   Kim, Chong Jai ^a,b,f   Kim, Yeon Mee ^a,b,g   Kim, Jung Sun ^a,b,h   Qureshi, Faisal ^a,b,e   Jacques, Suzanne M ^a,b,e   Yoon, Bo Hyun ^a,b,i   Chaiworapongsa, Tinnakorn ^a,b,e   Yeo, Lami ^a,b,e   Hassan, Sonia S ^a,b,e   Erez, Offer ^a,b,e   Korzeniewski, Steven J ^a,b,d,e  

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

^b University of Michigan ^*  (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f University of Ulsan College of Medicine   (South Korea)

^g Inje University College of Medicine   (South Korea)

^h Sungkyunkwan University School of Medicine   (South Korea)

ⁱ Seoul National University College of Medicine   (South Korea)

Author keywords

allograft; amniocentesis; biomarker; chorioamnionitis; chronic inflammation; cytokine; maternal anti fetal rejection

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLUCOSE; INTERLEUKIN 6; BIOLOGICAL MARKER; CXCL10 PROTEIN, HUMAN; IL6 PROTEIN, HUMAN;

ADULT; AMNIOCENTESIS; AMNION FLUID; AMNION FLUID ANALYSIS; ARTICLE; BIRTH WEIGHT; CHORIOAMNIONITIS; FEMALE; GESTATIONAL AGE; HUMAN; IMMUNOASSAY; LEUKOCYTE COUNT; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; PLACENTA DISORDER; PREGNANCY OUTCOME; PREMATURE FETUS MEMBRANE RUPTURE; PREMATURE LABOR; PRIORITY JOURNAL; RETROSPECTIVE STUDY; ACUTE DISEASE; CHRONIC DISEASE; IMMUNOLOGY; METABOLISM; PREGNANCY; YOUNG ADULT;

ACUTE DISEASE; ADULT; AMNIOTIC FLUID; BIOMARKERS; CHEMOKINE CXCL10; CHORIOAMNIONITIS; CHRONIC DISEASE; FEMALE; HUMANS; INTERLEUKIN-6; OBSTETRIC LABOR, PREMATURE; PREGNANCY; RETROSPECTIVE STUDIES; YOUNG ADULT;

EID: 85019576616     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12685     Document Type: Article

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138. Figueroa R, Garry D, Elimian A, Patel K, Sehgal PB, Tejani N. Evaluation of amniotic fluid cytokines in preterm labor and intact membranes. J Matern Fetal Neonatal Med. 2005;18:241-247.
139. Witt A, Berger A, Gruber CJ, Petricevic L, Apfalter P, Husslein P. IL-8 concentrations in maternal serum, amniotic fluid and cord blood in relation to different pathogens within the amniotic cavity. J Perinat Med. 2005;33:22-26.
140. Cobo T, Kacerovsky M, Palacio M, et al. Intra-amniotic inflammatory response in subgroups of women with preterm prelabor rupture of the membranes. PLoS One. 2012;7:e43677.
141. Romero R, Brody DT, Oyarzun E, et al. Infection and labor. III. Interleukin-1: a signal for the onset of parturition. Am J Obstet Gynecol. 1989;160:1117-1123.
142. Mitchell MD, Edwin SS, Silver RM, Romero RJ. Potential agonist action of the interleukin-1 receptor antagonist protein: implications for treatment of women. J Clin Endocrinol Metab. 1993;76:1386-1388.
143. Romero R, Manogue KR, Mitchell MD, et al. Infection and labor. IV. Cachectin-tumor necrosis factor in the amniotic fluid of women with intraamniotic infection and preterm labor. Am J Obstet Gynecol. 1989;161:336-341.
144. Romero R, Mazor M, Sepulveda W, Avila C, Copeland D, Williams J. Tumor necrosis factor in preterm and term labor. Am J Obstet Gynecol. 1992;166:1576-1587.
145. Sadowsky DW, Adams KM, Gravett MG, Witkin SS, Novy MJ. Preterm labor is induced by intraamniotic infusions of interleukin-1beta and tumor necrosis factor-alpha but not by interleukin-6 or interleukin-8 in a nonhuman primate model. Am J Obstet Gynecol. 2006;195:1578-1589.
146. Athayde N, Romero R, Maymon E, et al. Interleukin 16 in pregnancy, parturition, rupture of fetal membranes, and microbial invasion of the amniotic cavity. Am J Obstet Gynecol. 2000;182:135-141.
147. Pacora P, Romero R, Maymon E, et al. Participation of the novel cytokine interleukin 18 in the host response to intra-amniotic infection. Am J Obstet Gynecol. 2000;183:1138-1143.
148. Greig PC, Herbert WN, Robinette BL, Teot LA. Amniotic fluid interleukin-10 concentrations increase through pregnancy and are elevated in patients with preterm labor associated with intrauterine infection. Am J Obstet Gynecol. 1995;173:1223-1227.
149. Gotsch F, Romero R, Kusanovic JP, et al. The anti-inflammatory limb of the immune response in preterm labor, intra-amniotic infection/inflammation, and spontaneous parturition at term: a role for interleukin-10. J Matern Fetal Neonatal Med. 2008;21:529-547.
150. Maymon E, Romero R, Pacora P, et al. Human neutrophil collagenase (matrix metalloproteinase 8) in parturition, premature rupture of the membranes, and intrauterine infection. Am J Obstet Gynecol. 2000;183:94-99.
151. Maymon E, Romero R, Chaiworapongsa T, et al. Amniotic fluid matrix metalloproteinase-8 in preterm labor with intact membranes. Am J Obstet Gynecol. 2001;185:1149-1155.
152. Angus SR, Segel SY, Hsu CD, et al. Amniotic fluid matrix metalloproteinase-8 indicates intra-amniotic infection. Am J Obstet Gynecol. 2001;185:1232-1238.
153. Nien JK, Yoon BH, Espinoza J, et al. A rapid MMP-8 bedside test for the detection of intra-amniotic inflammation identifies patients at risk for imminent preterm delivery. Am J Obstet Gynecol. 2006;195:1025-1030.
154. Kim KW, Romero R, Park HS, et al. A rapid matrix metalloproteinase-8 bedside test for the detection of intraamniotic inflammation in women with preterm premature rupture of membranes. Am J Obstet Gynecol. 2007;197:292 e291-292 e295.
155. Park CW, Lee SM, Park JS, Jun JK, Romero R, Yoon BH. The antenatal identification of funisitis with a rapid MMP-8 bedside test. J Perinat Med. 2008;36:497-502.
156. Park CW, Yoon BH, Kim SM, Park JS, Jun JK. The frequency and clinical significance of intra-amniotic inflammation defined as an elevated amniotic fluid matrix metalloproteinase-8 in patients with preterm labor and low amniotic fluid white blood cell counts. Obstet Gynecol Sci. 2013;56:167-175.
157. Maymon E, Romero R, Pacora P, et al. Evidence for the participation of interstitial collagenase (matrix metalloproteinase 1) in preterm premature rupture of membranes. Am J Obstet Gynecol. 2000;183:914-920.
158. Maymon E, Romero R, Pacora P, et al. A role for the 72 kDa gelatinase (MMP-2) and its inhibitor (TIMP-2) in human parturition, premature rupture of membranes and intraamniotic infection. J Perinat Med. 2001;29:308-316.
159. Park KH, Chaiworapongsa T, Kim YM, et al. Matrix metalloproteinase 3 in parturition, premature rupture of the membranes, and microbial invasion of the amniotic cavity. J Perinat Med. 2003;31:12-22.
160. Maymon E, Romero R, Pacora P, et al. Matrilysin (matrix metalloproteinase 7) in parturition, premature rupture of membranes, and intrauterine infection. Am J Obstet Gynecol. 2000;182:1545-1553.
161. Locksmith GJ, Clark P, Duff P, Schultz GS. Amniotic fluid matrix metalloproteinase-9 levels in women with preterm labor and suspected intra-amniotic infection. Obstet Gynecol. 1999;94:1-6.
162. Maymon E, Romero R, Pacora P, et al. Evidence of in vivo differential bioavailability of the active forms of matrix metalloproteinases 9 and 2 in parturition, spontaneous rupture of membranes, and intra-amniotic infection. Am J Obstet Gynecol. 2000;183:887-894.
163. Harirah H, Donia SE, Hsu CD. Amniotic fluid matrix metalloproteinase-9 and interleukin-6 in predicting intra-amniotic infection. Obstet Gynecol. 2002;99:80-84.
164. Jacobsson B, Holst RM, Wennerholm UB, Andersson B, Lilja H, Hagberg H. 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;189:1161-1167.
165. 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;17:365-373.
166. Kacerovsky M, Celec P, Vlkova B, et al. Amniotic fluid protein profiles of intraamniotic inflammatory response to Ureaplasma spp. and other bacteria. PLoS One. 2013;8:e60399.
167. Jacobsson B, Holst RM, Andersson B, Hagberg H. 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;84:566-571.
168. 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;60:246-257.
169. Gervasi MT, Romero R, Bracalente G, et al. Midtrimester amniotic fluid concentrations of interleukin-6 and interferon-gamma-inducible protein-10: evidence for heterogeneity of intra-amniotic inflammation and associations with spontaneous early (<32 weeks) and late (>32 weeks) preterm delivery. J Perinat Med. 2012;40:329-343.
170. 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;21:763-775.
171. 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;9:535-540.
172. Chaiworapongsa T, Romero R, Espinoza J, et al. Macrophage migration inhibitory factor in patients with preterm parturition and microbial invasion of the amniotic cavity. J Matern Fetal Neonatal Med. 2005;18:405-416.
173. Athayde N, Romero R, Maymon E, et al. A role for the novel cytokine RANTES in pregnancy and parturition. Am J Obstet Gynecol. 1999;181:989-994.
174. 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 intra-amniotic infection and preterm delivery. Biol Reprod. 2004;70:253-259.
175. 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;35:23-29.
176. 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;37:503-511.
177. Andrys C, Kacerovsky M, Drahosova M, et al. Amniotic fluid soluble Toll-like receptor 2 in pregnancies complicated by preterm prelabor rupture of membranes. J Matern Fetal Neonatal Med. 2013;26:520-527.
178. Stampalija T, Chaiworapongsa T, Romero R, et al. Soluble ST2, a modulator of the inflammatory response, in preterm and term labor. J Matern Fetal Neonatal Med. 2014;27:111-121.
179. Park SP, Kim SA. Abstract No 322: The value of the genedia MMP-8 rapid test for diagnosing intraamniotic infection/inflammation and predicting adverse pregnancy outcomes in women with preterm premature rupture of membranes. Am J Obstet Gynecol. 2015;212:S174.
180. Park JY, Romero R, Lee J, Chaemsaithong P, Chaiyasit N, Yoon BH. An elevated amniotic fluid prostaglandin F2a concentration is associated with intra-amniotic inflammation/infection, clinical and histologic chorioamnionitis as well as impending preterm delivery in patients with preterm labor and intact membranes. J Matern Fetal Neonatal Med. 2016;29:2563-2572.
181. Romero R, Grivel JC, Tarca AL, et al. Evidence of perturbations of the cytokine network in preterm labor. Am J Obstet Gynecol. 2015;213:836 e831-836 e818.
182. Blanc WA. Pathology of the placenta and cord in ascending and in haematogenous infection. Ciba Found Symp. 1979;17-38.
183. Russell P. Inflammatory lesions of the human placenta: clinical significance of acute chorioamnionitis. Am J Diagn Gynecol Obstet. 1979;2:127-137.
184. Hillier SL, Martius J, Krohn M, Kiviat N, Holmes KK, Eschenbach DA. A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med. 1988;319:972-978.
185. Salafia CM, Weigl C, Silberman L. The prevalence and distribution of acute placental inflammation in uncomplicated term pregnancies. Obstet Gynecol. 1989;73:383-389.
186. Salafia CM, Vogel CA, Vintzileos AM, Bantham KF, Pezzullo J, Silberman L. Placental pathologic findings in preterm birth. Am J Obstet Gynecol. 1991;165:934-938.
187. Romero R, Salafia CM, Athanassiadis AP, et al. The relationship between acute inflammatory lesions of the preterm placenta and amniotic fluid microbiology. Am J Obstet Gynecol. 1992;166:1382-1388.
188. Redline RW, Faye-Petersen O, Heller D, Qureshi F, Savell V, Vogler C. Amniotic infection syndrome: nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol. 2003;6:435-448.
189. Redline RW. Placental inflammation. Semin Neonatol. 2004;9:265-274.
190. Redline RW. Infections and other inflammatory conditions. Semin Diagn Pathol. 2007;24:5-13.
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194. Torricelli M, Voltolini C, Toti P, et al. Histologic chorioamnionitis: different histologic features at different gestational ages. J Matern Fetal Neonatal Med. 2014;27:910-913.
195. Kim SM, Romero R, Park JW, Oh KJ, Jun JK, Yoon BH. The relationship between the intensity of intra-amniotic inflammation and the presence and severity of acute histologic chorioamnionitis in preterm gestation. J Matern Fetal Neonatal Med. 2015;28:1500-1509.
196. Kim CJ, Romero R, Chaemsaithong P, Chaiyasit N, Yoon BH, Kim YM. Acute chorioamnionitis and funisitis: definition, pathologic features, and clinical significance. Am J Obstet Gynecol. 2015;213:S29-S52.
197. 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.
198. Kim CJ, Yoon BH, Park SS, Kim MH, Chi JG. Acute funisitis of preterm but not term placentas is associated with severe fetal inflammatory response. Hum Pathol. 2001;32:623-629.
199. Kim EN, Kim CJ, Park JW, Yoon BH. Acute funisitis is associated with distinct changes in fetal hematologic profile. J Matern Fetal Neonatal Med. 2015;28:588-593.
200. Lee J, Oh KJ, Park CW, Park JS, Jun JK, Yoon BH. The presence of funisitis is associated with a decreased risk for the development of neonatal respiratory distress syndrome. Placenta. 2011;32:235-240.
201. Lee J, Romero R, Kim SM, et al. A new anti-microbial combination prolongs the latency period, reduces acute histologic chorioamnionitis as well as funisitis, and improves neonatal outcomes in preterm PROM. J Matern Fetal Neonatal Med. 2016;29:707-720.
202. Mi Lee S, Romero R, Lee KA, et al. The frequency and risk factors of funisitis and histologic chorioamnionitis in pregnant women at term who delivered after the spontaneous onset of labor. J Matern Fetal Neonatal Med. 2011;24:37-42.
203. Yoon BH, Romero R, Shim JY, Shim SS, Kim CJ, Jun JK. 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.
204. Park CW, Park JS, Moon KC, Jun JK, Yoon BH. Preterm labor and preterm premature rupture of membranes have a different pattern in the involved compartments of acute histologoic chorioamnionitis and/or funisitis: patho-physiologic implication related to different clinical manifestations. Pathol Int. 2016;66:325-332.
205. Romero R, Miranda J, Chaiworapongsa T, et al. A novel molecular microbiologic technique for the rapid diagnosis of microbial invasion of the amniotic cavity and intra-amniotic infection in preterm labor with intact membranes. Am J Reprod Immunol. 2014;71:330-358.
206. Romero R, Miranda J, Chaiworapongsa T, et al. Sterile intra-amniotic inflammation in asymptomatic patients with a sonographic short cervix: prevalence and clinical significance. J Matern Fetal Neonatal Med. 2014;1-17.
207. Romero R, Miranda J, Chaemsaithong P, et al. Sterile and microbial-associated intra-amniotic inflammation in preterm prelabor rupture of membranes. J Matern Fetal Neonatal Med. 2015;28:1394-1409.
208. Romero R, Miranda J, Kusanovic JP, et al. Clinical chorioamnionitis at term I: microbiology of the amniotic cavity using cultivation and molecular techniques. J Perinat Med. 2015;43:19-36.
209. Musilova I, Kutova R, Pliskova L, et al. Intraamniotic Inflammation in Women with Preterm Prelabor Rupture of Membranes. PLoS One. 2015;10:e0133929.
210. Hecht JL, Fichorova RN, Tang VF, Allred EN, McElrath TF, Leviton A. Relationship between neonatal blood protein concentrations and placenta histologic characteristics in extremely low GA newborns. Pediatr Res. 2011;69:68-73.
211. Committee opinion no 611: method for estimating due date. Obstet Gynecol. 2014;124:863-866.
212. Madan I, Romero R, Kusanovic JP, et al. The frequency and clinical significance of intra-amniotic infection and/or inflammation in women with placenta previa and vaginal bleeding: an unexpected observation. J Perinat Med. 2010;38:275-279.
213. DiGiulio DB, Gervasi M, Romero R, et al. Microbial invasion of the amniotic cavity in preeclampsia as assessed by cultivation and sequence-based methods. J Perinat Med. 2010;38:503-513.
214. Romero R, Chaiworapongsa T, Alpay Savasan Z, et al. Damage-associated molecular patterns (DAMPs) in preterm labor with intact membranes and preterm PROM: a study of the alarmin HMGB1. J Matern Fetal Neonatal Med. 2011;24:1444-1455.
215. Park KH, Kim SN, Oh KJ, Lee SY, Jeong EH, Ryu A. Noninvasive prediction of intra-amniotic infection and/or inflammation in preterm premature rupture of membranes. Reprod Sci. 2012;19:658-665.
216. Redline RW. Inflammatory responses in the placenta and umbilical cord. Semin Fetal Neonatal Med. 2006;11:296-301.
217. Redline RW. Classification of placental lesions. Am J Obstet Gynecol. 2015;213:S21-S28.
218. Kim JS, Romero R, Kim MR, et al. Involvement of Hofbauer cells and maternal T cells in villitis of unknown aetiology. Histopathology. 2008;52:457-464.
219. Redline RW. Villitis of unknown etiology: noninfectious chronic villitis in the placenta. Hum Pathol. 2007;38:1439-1446.
220. Khong TY, Bendon RW, Qureshi F, et al. Chronic deciduitis in the placental basal plate: definition and interobserver reliability. Hum Pathol. 2000;31:292-295.
221. Romero R, Mazor M, Wu YK, et al. Infection in the pathogenesis of preterm labor. Semin Perinatol. 1988;12:262-279.
222. Romero R, Mazor M. Infection and preterm labor. Clin Obstet Gynecol. 1988;31:553-584.
223. Romero R, Sirtori M, Oyarzun E, et al. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am J Obstet Gynecol. 1989;161:817-824.
224. Gomez R, Romero R, Edwin SS, David C. Pathogenesis of preterm labor and preterm premature rupture of membranes associated with intraamniotic infection. Infect Dis Clin North Am. 1997;11:135-176.
225. Romero R, Gomez R, Chaiworapongsa T, Conoscenti G, Kim JC, Kim YM. The role of infection in preterm labour and delivery. Paediatr Perinat Epidemiol. 2001;15(Suppl 2):41-56.
226. Romero R, Espinoza J, Chaiworapongsa T, Kalache K. Infection and prematurity and the role of preventive strategies. Semin Neonatol. 2002;7:259-274.
227. Leigh J, Garite TJ. Amniocentesis and the management of premature labor. Obstet Gynecol. 1986;67:500-506.
228. Romero R, Avila C, Brekus CA, Morotti R. The role of systemic and intrauterine infection in preterm parturition. Ann N Y Acad Sci. 1991;622:355-375.
229. Gauthier DW, Meyer WJ, Bieniarz A. Correlation of amniotic fluid glucose concentration and intraamniotic infection in patients with preterm labor or premature rupture of membranes. Am J Obstet Gynecol. 1991;165:1105-1110.
230. Coultrip LL, Grossman JH. Evaluation of rapid diagnostic tests in the detection of microbial invasion of the amniotic cavity. Am J Obstet Gynecol. 1992;167:1231-1242.
231. Watts DH, Krohn MA, Hillier SL, Eschenbach DA. The association of occult amniotic fluid infection with gestational age and neonatal outcome among women in preterm labor. Obstet Gynecol. 1992;79:351-357.
232. Coultrip LL, Lien JM, Gomez R, Kapernick P, Khoury A, Grossman JH. The value of amniotic fluid interleukin-6 determination in patients with preterm labor and intact membranes in the detection of microbial invasion of the amniotic cavity. Am J Obstet Gynecol. 1994;171:901-911.
233. Goncalves LF, Chaiworapongsa T, Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev. 2002;8:3-13.
234. Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel L, Hassan S. The role of inflammation and infection in preterm birth. Semin Reprod Med. 2007;25:21-39.
235. Romero R, Quintero R, Oyarzun E, et al. Intraamniotic infection and the onset of labor in preterm premature rupture of the membranes. Am J Obstet Gynecol. 1988;159:661-666.
236. Romero R, Ghidini A, Mazor M, Behnke E. Microbial invasion of the amniotic cavity in premature rupture of membranes. Clin Obstet Gynecol. 1991;34:769-778.
237. Romero R, Gonzalez R, Sepulveda W, et al. Infection and labor. VIII. Microbial invasion of the amniotic cavity in patients with suspected cervical incompetence: prevalence and clinical significance. Am J Obstet Gynecol. 1992;167:1086-1091.
238. Romero R, Avila C, Sepulveda W, et al. The role of systemic and intrauterine infection in preterm labor. In: Fuchs A, Fuchs F, Stubblefield P, eds. Preterm Birth: Causes, Prevention, and Management. New York: McGraw-Hill Inc.; 1993:97.
239. Matzinger P. The danger model: a renewed sense of self. Science. 2002;296:301-305.
240. Oppenheim JJ, Yang D. Alarmins: chemotactic activators of immune responses. Curr Opin Immunol. 2005;17:359-365.
241. Harris HE, Raucci A. Alarmin(g) news about danger: workshop on innate danger signals and HMGB1. EMBO Rep. 2006;7:774-778.
242. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol. 2007;81:1-5.
243. 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;36:388-398.
244. Gotsch F, Romero R, Chaiworapongsa T, et al. Evidence of the involvement of caspase-1 under physiologic and pathologic cellular stress during human pregnancy: a link between the inflammasome and parturition. J Matern Fetal Neonatal Med. 2008;21:605-616.
245. 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;21:449-461.
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249. Nunez G. Intracellular sensors of microbes and danger. Immunol Rev. 2011;243:5-8.
250. Romero R, Chaiworapongsa T, Savasan ZA, et al. Clinical chorioamnionitis is characterized by changes in the expression of the alarmin HMGB1 and one of its receptors, sRAGE. J Matern Fetal Neonatal Med. 2012;25:558-567.
251. Bredeson S, DeFord J, Yin H, Papaconstantinou J, Saade G, Menon R. Abstract No. 710: Acetylated HMGB1 in human amniotic fluid as an important factor in premature preterm rupture of the membranes. Am J Obstet Gynecol. 2014;2010:S348.
252. Ahmed AI, Chaemsaithong P, Chaiworapongsa T, et al. Abstract No. 599: A receptor for danger signals, advanced glycation and products (RAGE) in fetal inflammation and clinical chorioamnionitis. Am J Obstet Gynecol. 2015;212:S298.
253. Behnia F, Taylor BD, Woodson M, et al. Chorioamniotic membrane senescence: a signal for parturition? Am J Obstet Gynecol. 2015;213:359 e351-359 e316.
254. Behnia F, Saade G, Micheal V, et al. Abstract No. 98: Term fetal membranes and senescence associated secretory phenotype (SASP)-like gene expression: a signal for parturition? Am J Obstet Gynecol. 2015;212:S66.
255. Polettini J, Dutta E, Kechichian T, et al. Abstract No. 73: Activation of p38MAPK and senescence in fetal membranes induced by telomere overhang sequence: a novel mechanism for preterm birth. Am J Obstet Gynecol. 2015;212:S51.
256. Dutta E, Kacerovsky M, Behnia F, Kechichian T, Saade G, Menon R. Abstract No. 152: Development of DNA damage foci, loss of lamin B and activation of pp38MAPK: classic signs of senescence in human amniochorion. Am J Obstet Gynecol. 2015;212:S92.
257. Montenegro D, Romero R, Pineles BL, et al. Differential expression of the inflammasome components in the fetal inflammatory response syndrome. Reprod Sci. 2007;14:59A-60A.
258. Pineles BL, Romero R, Montenegro D, et al. The inflammasome in human parturition. Reprod Sci. 2007;14:59A.
259. Abrahams VM. The role of the Nod-like receptor family in trophoblast innate immune responses. J Reprod Immunol. 2011;88:112-117.
260. Lappas M. Caspase-1 activation is increased with human labour in foetal membranes and myometrium and mediates infection-induced interleukin-1beta secretion. Am J Reprod Immunol. 2014;71:189-201.
261. Romero R, Gomez-Lopez N, Xu Y, et al. A role of inflammasome in spontaneous labor at term. Abstract presented at 12th World Congress of Perinatal Medicine, 3rd-6th November, 2015, Madrid, Spain; 2015.
262. Gomez-Lopez N, Romero R, Plazyo O, et al. Intra-amniotic administration of HMGB1 induces spontaneous preterm labor and birth. Am J Reprod Immunol. 2016;75:3-7.
263. Plazyo O, Romero R, Unkel R, et al. HMGB1 induces an inflammatory response in the chorioamniotic membranes that is partially mediated by the inflammasome. Biol Reprod. 2016;95:130.
264. 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;32:108-113.
265. Dudley DJ, Hunter C, Mitchell MD, Varner MW. Elevations of amniotic fluid macrophage inflammatory protein-1 alpha concentrations in women during term and preterm labor. Obstet Gynecol. 1996;87:94-98.
266. 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.
267. Wei SQ, Fraser W, Luo ZC. Inflammatory cytokines and spontaneous preterm birth in asymptomatic women: a systematic review. Obstet Gynecol. 2010;116:393-401.
268. Conde-Agudelo A, Papageorghiou AT, Kennedy SH, Villar J. Novel biomarkers for the prediction of the spontaneous preterm birth phenotype: a systematic review and meta-analysis. BJOG. 2011;118:1042-1054.
269. Romero R, Grivel JC, Tarca AL, et al. Evidence of perturbations of the cytokine network in preterm labor. Am J Obstet Gynecol. 2015;213:836.e1-836.e18.
270. Rotondi M, Rosati A, Buonamano A, et al. High pretransplant serum levels of CXCL10/IP-10 are related to increased risk of renal allograft failure. Am J Transplant. 2004;4:1466-1474.
271. Hoffman SA, Wang L, Shah CV, et al. Plasma cytokines and chemokines in primary graft dysfunction post-lung transplantation. Am J Transplant. 2009;9:389-396.
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