A point of care test for interleukin-6 in amniotic fluid in preterm prelabor rupture of membranes: A step toward the early treatment of acute intra-amniotic inflammation/infection

Journal of Maternal-Fetal and Neonatal Medicine

Volumn 29, Issue 3, 2016, Pages 360-367

  Chaemsaithong, Piya ^a,b   Romero, Roberto ^a,c,d   Korzeniewski, Steven J ^a,b,d   Martinez Varea, Alicia ^a,b   Dong, Zhong ^a,b   Yoon, Bo Hyun ^e   Hassan, Sonia S ^a,b   Chaiworapongsa, Tinnakorn ^a,b   Yeo, Lami ^a,b  

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

^b WAYNE STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e Seoul National University   (South Korea)

Author keywords

Acute chorioamnionitis; acute funisitis; amniocentesis; biomarkers; ELISA; microbial invasion of the amniotic cavity; preterm labor; rapid interleukin 6

Indexed keywords

INTERLEUKIN 6; IL6 PROTEIN, HUMAN;

ADULT; AEROBIC BACTERIUM; AMNIOCENTESIS; AMNION; AMNION FLUID ANALYSIS; ANAEROBIC BACTERIUM; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; IMMUNOASSAY; INTERMETHOD COMPARISON; KOLMOGOROV SMIRNOV TEST; MAJOR CLINICAL STUDY; OUTCOME ASSESSMENT; POINT OF CARE TESTING; PREDICTIVE VALUE; PREMATURE FETUS MEMBRANE RUPTURE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SENSITIVITY AND SPECIFICITY; SPECIES CULTIVATION; AMNION FLUID; CHEMISTRY; CHORIOAMNIONITIS; POINT OF CARE SYSTEM; PREGNANCY; PREGNANCY OUTCOME; YOUNG ADULT;

ADULT; AMNIOTIC FLUID; CHORIOAMNIONITIS; FEMALE; FETAL MEMBRANES, PREMATURE RUPTURE; HUMANS; INTERLEUKIN-6; POINT-OF-CARE SYSTEMS; PREGNANCY; PREGNANCY OUTCOME; RETROSPECTIVE STUDIES; YOUNG ADULT;

EID: 84951073638     PISSN: 14767058     EISSN: 14764954     Source Type: Journal    
DOI: 10.3109/14767058.2015.1006621     Document Type: Article

References (114)

1. Romero R, Yeo L, Gotsch F, et al. Prelabor rupture of the membranes. In: Winn HN, Chervanak FA, Romero R., eds. Clinical maternal-fetal medicine online. 2nd ed. UK: Informa Healthcare; 2011: 1-24
2. Parry S, Strauss JF III. Premature rupture of the fetal membranes. N Engl J Med 1998; 338: 663-70
3. Mercer BM. Preterm premature rupture of the membranes: current approaches to evaluation and management. Obstet Gynecol Clin North Am 2005; 32: 411-28
4. Kenyon S, Boulvain M, Neilson JP. Antibiotics for preterm rupture of membranes. Cochrane Database Syst Rev 2013; 12: CD001058
5. Santolaya-Forgas J, Romero R, Espinoza J, et al. Prelabour rupture of the membranes. In: Reece EA, Hobbins JC., eds. Clinical obstetrics the fetus & mothers. 3rd ed. Malden (MA): Blackwell; 2008: 1130-88
6. Romero R, Dey SK, Fisher SJ. Preterm labor: one syndrome, many causes. Science 2014; 345: 760-5
7. Ladfors L, Mattsson LA, Eriksson M, Milsom I. Prevalence and risk factors for prelabor rupture of the membranes (PROM) at or near-term in an urban Swedish population. J Perinat Med 2000; 28: 491-6
8. Ismail AQ, Lahiri S. Management of prelabour rupture of membranes (PROM) at term. J Perinat Med 2013; 41: 647-9
9. Grunebaum A. Reply to Management of prelabour rupture of membranes (PROM) at term. J Perinat Med 2013; 41: 651-2
10. Eschenbach D. Reply to: Ismail AQT, Lahiri S. Management of prelabor rupture of membranes (PROM) at term. J Perinat Med 2013; 41: 653-5
11. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet 2008; 371: 75-84
12. Daikoku NH, Kaltreider DF, Khouzami VA, et al. Premature rupture of membranes and spontaneous preterm labor: maternal endometritis risks. Obstet Gynecol 1982; 59: 13-20
13. Manuck TA, Maclean CC, Silver RM, Varner MW. Preterm premature rupture of membranes: does the duration of latency influence perinatal outcomes? Am J Obstet Gynecol 2009; 201: 414.e1-6
14. Deutsch A, Deutsch E, Totten C, et al. Maternal and neonatal outcomes based on the gestational age of midtrimester preterm premature rupture of membranes. J Matern Fetal Neonatal Med 2010; 23: 1429-34
15. Gulati S, Agrawal S, Raghunandan C, et al. Maternal serum interleukin-6 and its association with clinicopathological infectious morbidity in preterm premature rupture of membranes: a prospective cohort study. J Matern Fetal Neonatal Med 2012; 25: 1428-32
16. Tsiartas P, Kacerovsky M, Musilova I, et al. The association between histological chorioamnionitis, funisitis and neonatal outcome in women with preterm prelabor rupture of membranes. J Matern Fetal Neonatal Med 2013; 26: 1332-6
17. Acaia B, Crovetto F, Ossola MW, et al. Predictive factors for neonatal survival in women with periviable preterm rupture of the membranes. J Matern Fetal Neonatal Med 2013; 26: 1628-34
18. Manuck TA, Sheng X, Yoder BA, Varner MW. Correlation between initial neonatal and early childhood outcomes following preterm birth. Am J Obstet Gynecol 2014; 210: 426.e1-9
19. Manuck TA, Varner MW. Neonatal and early childhood outcomes following early vs later preterm premature rupture of membranes. Am J Obstet Gynecol 2014; 211: 308.e1-6
20. Cotton DB, Hill LM, Strassner HT, et al. Use of amniocentesis in preterm gestation with ruptured membranes. Obstet Gynecol 1984; 63: 38-43
21. Zlatnik FJ, Cruikshank DP, Petzold CR, Galask RP. Amniocentesis in the identification of inapparent infection in preterm patients with premature rupture of the membranes. J Reprod Med 1984; 29: 656-60
22. Broekhuizen FF, Gilman M, Hamilton PR. Amniocentesis for gram stain and culture in preterm premature rupture of the membranes. Obstet Gynecol 1985; 66: 316-21
23. Feinstein SJ, Vintzileos AM, Lodeiro JG, et al. Amniocentesis with premature rupture of membranes. Obstet Gynecol 1986; 68: 147-52
24. Romero R, Emamian M, Wan M, et al. The value of the leukocyte esterase test in diagnosing intra-amniotic infection. Am J Perinatol 1988; 5: 64-9
25. Dudley J, Malcolm G, Ellwood D. Amniocentesis in the management of preterm premature rupture of the membranes. Aust N Z J Obstet Gynaecol 1991; 31: 331-6
26. 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
27. Font GE, Gauthier DW, Meyer WJ, et al. Catalase activity as a predictor of amniotic fluid culture results in preterm labor or premature rupture of membranes. Obstet Gynecol 1995; 85: 656-8
28. Yoon BH, Jun JK, Park KH, et al. Serum C-reactive protein, white blood cell count, and amniotic fluid white blood cell count in women with preterm premature rupture of membranes. Obstet Gynecol 1996; 88: 1034-40
29. Blackwell SC, Berry SM. Role of amniocentesis for the diagnosis of subclinical intra-amniotic infection in preterm premature rupture of the membranes. Curr Opin Obstet Gynecol 1999; 11: 541-7
30. Oh KJ, Lee KA, Sohn YK, et al. Intraamniotic infection with genital mycoplasmas exhibits a more intense inflammatory response than intraamniotic infection with other microorganisms in patients with preterm premature rupture of membranes. Am J Obstet Gynecol 2010; 203: 211.e1-8
31. Cobo T, Palacio M, Martinez-Terron M, et al. Clinical and inflammatory markers in amniotic fluid as predictors of adverse outcomes in preterm premature rupture of membranes. Am J Obstet Gynecol 2011; 205: 126.e1-8
32. Kacerovsky M, Musilova I, Khatibi A, et al. Intraamniotic inflammatory response to bacteria: analysis of multiple amniotic fluid proteins in women with preterm prelabor rupture of membranes. J Matern Fetal Neonatal Med 2012; 25: 2014-19
33. Kacerovsky M, Cobo T, Andrys C, et al. The fetal inflammatory response in subgroups of women with preterm prelabor rupture of the membranes. J Matern Fetal Neonatal Med 2013; 26: 795-801
34. Kacerovsky M, Musilova I, Andrys C, et al. Prelabor rupture of membranes between 34 and 37 weeks: the intraamniotic inflammatory response and neonatal outcomes. Am J Obstet Gynecol 2014; 210: 325.e1-e10
35. DiGiulio DB, Romero R, Kusanovic JP, et al. 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
36. 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 2014;1-16. [Epub ahead of print]. doi: 10.3109/14767058.2014.958463
37. 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: 661-6
38. Shim SS, Romero R, Hong JS, et al. Clinical significance of intra-amniotic inflammation in patients with preterm premature rupture of membranes. Am J Obstet Gynecol 2004; 191: 1339-45
39. 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: 330-58
40. 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; 72: 458-74
41. 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. [Epub ahead of print]. doi: 10.3109/14767058.2014.954243
42. Romero R, Yoon BH, Kenney JS, et al. Amniotic fluid interleukin-6 determinations are of diagnostic and prognostic value in preterm labor. Am J Reprod Immunol 1993; 30: 167-83
43. Coultrip LL, Lien JM, Gomez R, et al. 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: 901-11
44. Greci LS, Gilson GJ, Nevils B, et al. Is amniotic fluid analysis the key to preterm labor? A model using interleukin-6 for predicting rapid delivery. Am J Obstet Gynecol 1998; 179: 172-8
45. El-Bastawissi AY, Williams MA, Riley DE, et al. Amniotic fluid interleukin-6 and preterm delivery: a review. Obstet Gynecol 2000; 95: 1056-64
46. Yoon BH, Romero R, Moon JB, et al. Clinical significance of intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2001; 185: 1130-6
47. Wei SQ, Fraser W, Luo ZC. Inflammatory cytokines and spontaneous preterm birth in asymptomatic women: a systematic review. Obstet Gynecol 2010; 116: 393-401
48. 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: 1042-54
49. 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
50. Meem M, Modak JK, Mortuza R, et al. Biomarkers for diagnosis of neonatal infections: a systematic analysis of their potential as a point-of-care diagnostics. J Glob Health 2011; 1: 201-9
51. Batfalsky A, Lohr A, Heussen N, et al. Diagnostic value of an interleukin-6 bedside test in term and preterm neonates at the time of clinical suspicion of early- and late-onset bacterial infection. Neonatology 2012; 102: 37-44
52. Schefold JC, Hasper D, von Haehling S, et al. Interleukin-6 serum level assessment using a new qualitative point-of-care test in sepsis: a comparison with ELISA measurements. Clin Biochem 2008; 41: 893-8
53. Dengler J, Schefold JC, Graetz D, et al. Point-of-care testing for interleukin-6 in cerebro spinal fluid (CSF) after subarachnoid haemorrhage. Med Sci Monit 2008; 14: BR265-8
54. Chaemsaithong P, Romero R, Korzeniewski SJ, et al. A point of care test for the determination of amniotic fluid interleukin-6 and the chemokine CXCL-10/IP-10. J Matern Fetal Neonatal Med 2014;1-10. [Epub ahead of print]. doi: 10.3109/14767058.2014.961417
55. Chaemsaithong P, Romero R, Korzeniewski SJ, et al. A rapid interleukin-6 bedside test for the identification of intra-amniotic inflammation in preterm labor with intact membranes. J Matern Fetal Neonatal Med (accepted). 2014. [Epub ahead of print
56. Vousden N, Chandiramani M, Seed P, Shennan A. Interleukin-6 bedside testing in women at high risk of preterm birth. J Matern Fetal Neonatal Med 2011; 24: 1301-4
57. Berthiaume M, Rousseau E, Rola-Pleszczynski M, Pasquier JC. Rapid evaluation of the absence of inflammation after rupture of membranes. J Matern Fetal Neonatal Med 2014; 27: 865-9
58. Kacerovsky M, Musilova I, Hornychova H, et al. Bedside assessment of amniotic fluid interleukin-6 in preterm prelabor rupture of membranes. Am J Obstet Gynecol 2014; 211: 385.e1-9
59. Gibbs RS, Blanco JD, St Clair PJ, Castaneda YS. Quantitative bacteriology of amniotic fluid from women with clinical intraamniotic infection at term. J Infect Dis 1982; 145: 1-8
60. Hauth JC, Gilstrap LC, III, Hankins GD, Connor KD. Term maternal and neonatal complications of acute chorioamnionitis. Obstet Gynecol 1985; 66: 59-62
61. Gibbs RS, Dinsmoor MJ, Newton ER, Ramamurthy RS. A randomized trial of intrapartum versus immediate postpartum treatment of women with intra-amniotic infection. Obstet Gynecol 1988; 72: 823-8
62. Redline RW, Heller D, Keating S, Kingdom J. Placental diagnostic criteria and clinical correlation- A workshop report. Placenta 2005; 26: S114-17
63. Redline RW. Inflammatory responses in the placenta and umbilical cord. Semin Fetal Neonatal Med 2006; 11: 296-301
64. 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
65. 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
66. 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 220-3
67. Andrews WW, Hauth JC, Goldenberg RL, et al. Amniotic fluid interleukin-6: correlation with upper genital tract microbial colonization and gestational age in women delivered after spontaneous labor versus indicated delivery. Am J Obstet Gynecol 1995; 173: 606-12
68. Yoon BH, Romero R, Kim CJ, et al. Amniotic fluid interleukin-6: a sensitive test for antenatal diagnosis of acute inflammatory lesions of preterm placenta and prediction of perinatal morbidity. Am J Obstet Gynecol 1995; 172: 960-70
69. Yoon BH, Romero R, Jun JK, et al. Amniotic fluid cytokines (interleukin-6, tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-8) and the risk for the development of bronchopulmonary dysplasia. Am J Obstet Gynecol 1997; 177: 825-30
70. 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
71. 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: 329-43
72. 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.e1-6
73. Combs CA, Gravett M, Garite TJ, et al. Amniotic fluid infection, inflammation, and colonization in preterm labor with intact membranes. Am J Obstet Gynecol 2014; 210: 125.e1-e15
74. 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 2014;43:19-36
75. Yoon BH, Romero R, Park JS, et al. Microbial invasion of the amniotic cavity with Ureaplasma urealyticum is associated with a robust host response in fetal, amniotic, and maternal compartments. Am J Obstet Gynecol 1998; 179: 1254-60
76. 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: 1124-9
77. Hillier SL, Martius J, Krohn M, et al. A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med 1988; 319: 972-8
78. Hillier SL, Krohn MA, Kiviat NB, et al. Microbiologic causes and neonatal outcomes associated with chorioamnion infection. Am J Obstet Gynecol 1991; 165: 955-61
79. 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: 1382-8
80. Arias F, Victoria A, Cho K, Kraus F. Placental histology and clinical characteristics of patients with preterm premature rupture of membranes. Obstet Gynecol 1997; 89: 265-71
81. Redline RW, Wilson-Costello D, Borawski E, et al. Placental lesions associated with neurologic impairment and cerebral palsy in very low-birth-weight infants. Arch Pathol Lab Med 1998; 122: 1091-8
82. Smulian JC, Vintzileos AM, Lai YL, et al. Maternal chorioamnionitis and umbilical vein interleukin-6 levels for identifying early neonatal sepsis. J Matern Fetal Med 1999; 8: 88-94
83. Redline RW, Wilson-Costello D, Borawski E, et al. The relationship between placental and other perinatal risk factors for neurologic impairment in very low birth weight children. Pediatr Res 2000; 47: 721-6
84. Dexter SC, Pinar H, Malee MP, et al. Outcome of very low birth weight infants with histopathologic chorioamnionitis. Obstet Gynecol 2000; 96: 172-7
85. Elimian A, Verma U, Beneck D, et al. Histologic chorioamnionitis, antenatal steroids, and perinatal outcomes. Obstet Gynecol 2000; 96: 333-6
86. Wu YW, Colford JM Jr. Chorioamnionitis as a risk factor for cerebral palsy: a meta-analysis. JAMA 2000; 284: 1417-24
87. Williams MC, O'Brien WF, Nelson RN, et al. Histologic chorioamnionitis is associated with fetal growth restriction in term and preterm infants. Am J Obstet Gynecol 2000; 183: 1094-9
88. Gaudet LM, Smith GN. Cerebral palsy and chorioamnionitis: the inflammatory cytokine link. Obstet Gynecol Surv 2001; 56: 433-6
89. 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: 623-9
90. 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
91. Holcroft CJ, Askin FB, Patra A, et al. Are histopathologic chorioamnionitis and funisitis associated with metabolic acidosis in the preterm fetus? Am J Obstet Gynecol 2004; 191: 2010-15
92. Choi CW, Kim BI, Park JD, et al. Risk factors for the different types of chronic lung diseases of prematurity according to the preceding respiratory distress syndrome. Pediatr Int 2005; 47: 417-23
93. Dempsey E, Chen MF, Kokottis T, et al. Outcome of neonates less than 30 weeks gestation with histologic chorioamnionitis. Am J Perinatol 2005; 22: 155-9
94. Andrews WW, Goldenberg RL, Faye-Petersen O, et al. The Alabama Preterm Birth study: polymorphonuclear and mononuclear cell placental infiltrations, other markers of inflammation, and outcomes in 23- to 32-week preterm newborn infants. Am J Obstet Gynecol 2006; 195: 803-8
95. Rocha G, Proenca E, Quintas C, et al. Chorioamnionitis and brain damage in the preterm newborn. J Matern Fetal Neonatal Med 2007; 20: 745-9
96. Holzman C, Lin X, Senagore P, Chung H. Histologic chorioamnionitis and preterm delivery. Am J Epidemiol 2007; 166: 786-94
97. Kallapur SG, Nitsos I, Moss TJ, et al. IL-1 mediates pulmonary and systemic inflammatory responses to chorioamnionitis induced by lipopolysaccharide. Am J Respir Crit Care Med 2009; 179: 955-61
98. Park CW, Moon KC, Park JS, et al. The involvement of human amnion in histologic chorioamnionitis is an indicator that a fetal and an intra-amniotic inflammatory response is more likely and severe: clinical implications. Placenta 2009; 30: 56-61
99. Menon R, Taylor RN, Fortunato SJ. Chorioamnionitis- A complex pathophysiologic syndrome. Placenta 2010; 31: 113-20
100. Hendson L, Russell L, Robertson CM, et al. Neonatal and neurodevelopmental outcomes of very low birth weight infants with histologic chorioamnionitis. J Pediatr 2011; 158: 397-402
101. Jobe AH. Effects of chorioamnionitis on the fetal lung. Clin Perinatol 2012; 39: 441-57
102. Martinelli P, Sarno L, Maruotti GM, et al. Chorioamnionitis and prematurity: a critical review. J Matern Fetal Neonatal Med 2012; 25: 29-31
103. Bersani I, Thomas W, Speer CP. Chorioamnionitis-the good or the evil for neonatal outcome? J Matern Fetal Neonatal Med 2012; 25: 12-16
104. Trevisanuto D, Peruzzetto C, Cavallin F, et al. Fetal placental inflammation is associated with poor neonatal growth of preterm infants: a case-control study. J Matern Fetal Neonatal Med 2013; 26: 1484-90
105. Kim SM, Romero R, Park JW, et al. 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 2014;1-10. [Epub ahead of print]. doi: 10.3109/14767058.2014.961009
106. Kallapur SG, Presicce P, Rueda CM, et al. Fetal immune response to chorioamnionitis. Semin Reprod Med 2014; 32: 56-67
107. Arayici S, Kadioglu Simsek G, Oncel MY, et al. The effect of histological chorioamnionitis on the short-term outcome of preterm infants
108. Vedovato S, Lo Iacono A, Morando C, et al. Sensorineural hearing loss in very low birth weight infants with histological chorioamnionitis. J Matern Fetal Neonatal Med 2014;1-5. [Epub ahead of print]. doi: 10.3109/14767058.2014.936375
109. Romero R, Mazor M, Wu YK, et al. Infection in the pathogenesis of preterm labor. Semin Perinatol 1988; 12: 262-79
110. Romero R, Mazor M. Infection and preterm labor. Clin Obstet Gynecol 1988; 31: 553-84
111. Romero R, Avila C, Santhanam U, et al. Amniotic fluid interleukin 6 in preterm labor. Association with infection. J Clin Invest 1990; 85: 1392-400
112. Goncalves LF, Chaiworapongsa T, Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev 2002; 8: 3-13
113. Yoon BH, Romero R, Moon J, et al. Differences in the fetal interleukin-6 response to microbial invasion of the amniotic cavity between term and preterm gestation. J Matern Fetal Neonatal Med 2003; 13: 32-8
114. 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.e1-5