Histological chorioamnionitis: Current concepts of diagnosis, classification and clinical significance

Fetal and Maternal Medicine Review

Volumn 22, Issue 1, 2011, Pages 25-44

  Jessop, F ^a   Sebire, N J ^b  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; DNA 16S; INTERLEUKIN 10; INTERLEUKIN 6; NEUTROPHIL COLLAGENASE; PENTRAXIN 3; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2;

ABDOMINAL TENDERNESS; BACTERIAL COLONIZATION; CANDIDIASIS; CELL DAMAGE; CEREBRAL PALSY; CHORIOAMNIONITIS; CLINICAL PRACTICE; DISEASE ASSOCIATION; ENCEPHALOMALACIA; FALSE NEGATIVE RESULT; FALSE POSITIVE RESULT; FEMALE GENITAL TRACT INFECTION; FETUS DEATH; FROZEN SECTION; FUNISITIS; FUSOBACTERIUM; GENETIC ASSOCIATION; HAEMOPHILUS INFLUENZAE; HISTOPATHOLOGY; HUMAN; HYPOXIA; INCIDENCE; INNATE IMMUNITY; LABORATORY DIAGNOSIS; MYCOPLASMA; MYCOSIS; NEISSERIA GONORRHOEAE; NEWBORN MORTALITY; OUTCOME ASSESSMENT; PATHOGENESIS; PELVIS ABSCESS; POINT OF CARE TESTING; POLYMERASE CHAIN REACTION; PREMATURE FETUS MEMBRANE RUPTURE; PREMATURE LABOR; REVIEW; SECOND TRIMESTER PREGNANCY; SPONTANEOUS ABORTION; STILLBIRTH; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PNEUMONIAE; TACHYCARDIA; TWIN PREGNANCY; UPREGULATION; UREAPLASMA; VAGINA DISCHARGE;

EID: 84862852389     PISSN: 09655395     EISSN: 14695065     Source Type: Journal    
DOI: 10.1017/S0965539511000015     Document Type: Review

References (126)

1. Speert H. Memorable medical mentors: V; Nicholson J Eastman. Obstet Gynecol Surv 2004; 59: 399-405.
2. William MD, Blanc P. Pathways of fetal and early neonatal infection: Viral placentitis, bacterial and fungal chorioamnionitis.J Pediatr 1961; 59: 473-96.
3. Fox H, Sebire NJ. Infections and inflammatory lesions of the placenta. Pathology of the Placenta 2007; Saunders, Elsevier, London, 303-354.
4. Hood M, Janney A, Dameron G. Beta hemolytic streptococcus group B associated with problems of the perinatal period. Am J Obstet Gynecol 1961; 82: 809-18.
5. Benirschke K, Kaufman P, Baergen RN. Pathology of the Human Placenta. 5th ed. 2006, New York: Springer, 657-760.
6. Lewis SH, Perrin E. Pathology of the Placenta. Churchill Livingstone, New York, 1999
7. Bobitt JR, Ledger WJ. Amniotic-fluid analysis-its role in maternal and neonatal infection. Obstet Gynecol 1978; 51: 56-62.
8. MacVicar J. Chorioamnionitis. Clin Obstet Gynecol 1970; 13: 272-90.
9. Bobitt JR, Ledger WJ. Unrecognized amnionitis and prematurity- preliminary-report. J Reprod Med 1977; 19: 8-12.
10. White CA, Longnecker DS. Leukocytic infiltration of the umbilical cord. Fetal infection or hypoxia? Obstet Gynecol 1967; 29: 711-18.
11. Olding L. Value of placentitis as a sign of intrauterine infection in human subjects. Acta Pathol Microbiol Scand 1970; 78: 256-64.
12. Dominguez R, Segal AJ, O'Sullivan JA. Leukocytic infiltration of the umbilical cord. Manifestation of fetal hypoxia due to reduction of blood flow in the cord. J Am Med Assoc 1960; 173: 346-49.
13. Seong HS, Lee SE, Kang JH, Romero R, Yoon BH. The frequency of microbial invasion of the amniotic cavity and histologic chorioamnionitis in women at term with intact membranes in the presence or absence of labor. Am J Obstet Gynecol 2008; 199: 375 e1-5.
14. Pettker CM, Buhimschi IA, Magloire LK, Sfakianaki AK, Hamar BD, Buhimschi CS. Value of placental microbial evaluation in diagnosing intra-amniotic infection. Obstet Gynecol 2007; 109: 739-749.
15. Satosar A, Ramirez NC, Bartholomew D, Davis J,Nuovo GJ. Histologic correlates of viral and bacterial infection of the placenta associated with severe morbidity and mortality in the newborn. Hum Pathol 2004; 35: 536-45.
16. Srinivas SK, Ernst LM, Edlow AG, Elovitz MA. Can placental pathology explain second-trimester pregnancy loss and subsequent pregnancy outcomes? Am J Obstet Gynecol 2008; 199: 402 e1-5.
17. Han YW, Shen T, Chung P, Buhimschi IA, Buhimschi CS. Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J Clin Microbiol 2009; 47: 38-47.
18. Jones HE, Harris KA, Azizia M, et al. Differing prevalence and diversity of bacterial species in fetal membranes from very preterm and term labor. PLOS One 2009; 4: e8205
19. Benirschke K. What pediatricians should know about the placenta. Current Prob Pediatr 1971; 2: 3-32.
20. Robbins SJ, Kumar V. Robbins & Cotran Pathologic Basis of Dis, Saunders, New York, 2009.
21. Anderson BL, Simhan HN, Simons KM, Wiesenfeld HC. Untreated asymptomatic group B streptococcal bacteriuria early in pregnancy and chorioamnionitis at delivery. Am J Obstet Gynecol 2007; 196: 524.e1-5.
22. Murray PE. Manual of Clinical Microbiology, 8th Ed. 2003, Washington: ASM Press.
23. Cassell GH, Waites KB, Watson HL, Crouse DT, Harasawa R. Ureaplasma-urealyticum intrauterine infection-role in prematurity and disease in newborns. Clin Microbiol Rev 1993; 6: 69-87.
24. Larsen B, Hwang J. Mycoplasma, ureaplasma, and adverse pregnancy outcomes: a fresh look. Infect Dis Obstet Gynecol 2010; 2010 pii: 521921.
25. Waites KB, Schelonka RL, Xiao L, Grigsby PL, Novy MJ. Congenital and opportunistic infections: Ureaplasma species and Mycoplasma hominis. Semin Fetal Neonatal Med 2009; 14: 190-99.
26. Berger A, Witt A, Haiden N, Kretzer V, Heinze G, Kohlhauser C. Microbial invasion of the amniotic cavity at birth is associated with adverse short-term outcome of preterm infants. J Perinat Med 2003; 31: 115-21.
27. Yoon BH, Chang JW, Romero R. Isolation of Ureaplasma urealyticum from the amniotic cavity and adverse outcome in preterm labor. Obstet Gynecol 1998; 92: 77-82.
28. Kirchner L, Helmer H, Heinze G, Wald M, Brunbauer M, Weninger M, Zaknun D. Amnionitis with Ureaplasma urealyticum or other microbes leads to increased morbidity and prolonged hospitalization in very low birth weight infants. Eur J Obstet Gynecol Reprod Biol 2007; 134: 44-50.
29. Jazayeri A, Lantz ME, O'Brien WF. Fusobacterium chorioamnionitis: report of two cases in preterm labour with intact amniotic membranes. Infect Dis Obstet Gynecol 1996; 4: 243-46.
30. Han YW, Ikegami A, Bissada NF, Herbst M, Redline RW, Ashmead GG. Transmission of an uncultivated Bergeyella strain from the oral cavity to amniotic fluid in a case of preterm birth. J Clin Microbiol 2006; 44: 1475-483.
31. Khader YS, Ta'ani Q. Periodontal diseases and the risk of preterm birth and low birth weight: a meta-analysis. J Periodontol 2005; 76: 161-65.
32. Jadhav AR, Belfort MA, Dildy GA. Eikenella corrodens chorioamnionitis: modes of infection? Am J Obstet Gynecol 2009; 200: e4-e5.
33. Schwartz DA, Reef S. Candida albicans placentitis and funisitis: early diagnosis of congenital candidemia by histopathologic examination of umbilical cord vessels. Pediatr Inf Dis J 1990; 9: 661-65.
34. Altshuler G. Pathogenesis of congenital herpes virus infection: case report including a description of the placenta. Am J Dis Child 1974; 127: 427-29.
35. Srinivas SK, Ma Y, Sammel MD, Chou D, McGrath C, Parry S, Elovitz MA. Placental inflammation and viral infection are implicated in second trimester pregnancy loss.AmJObstet Gynecol 2006; 195: 797-802.
36. MenonR, TaylorRN, Fortunato SJ.Chorioamnionitis; a complex pathophysiologic syndrome. Placenta 2010; 31: 113-20.
37. Ma Y, Krikun G, Abrahams VM,Mor G, Guller S. Cell type-specific expression and function of toll-like receptors 2 and 4 in human placenta: Implications in fetal infection. Placenta 2007; 28: 1024-1031.
38. Kacerovsky M, Tosner J, Drahosova M, Hornychova H, Andrys C. Pentraxin 3 in amniotic fluid as a marker of intra-amniotic inflammation in women with preterm premature rupture of membranes. Int J Gynecol Obstet 2010; 108: 203-206.
39. Buhimschi IA, Zhao G, Pettker CM, Bahtiyar MO, Magloire LK, Thung S et al. The receptor for advanced glycation end products (RAGE) system in women with intraamniotic infection and inflammation. Am J Obstet Gynecol 2007; 196: 181.e1-13.
40. Romero R, Espinoza J, Hassan S, Gotsch F, Kusanovic JP, Avila C 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.
41. Romero R, Velez Edwards DR, Kusanovic JP, Hassan SS, Mazaki-Tovi S, Vaisbuch E et al. Identification of fetal and maternal single nucleotide polymorphisms in candidate genes that predispose to spontaneous preterm labor with intact membranes. Am J Obstet Gynecol 2010; 202: 431.e1-34.
42. Romero R, Friel LA, Velez Edwards DR, Kusanovic JP, Hassan SS, Mazaki-Tovi S et al. A genetic association study of maternal and fetal candidate genes that predispose to preterm prelabor rupture of membranes (PROM). Am J Obstet Gynecol 2010 203: 361.e1-e30.
43. Lee SD, Kim MR, Hwang PG, Shim SS, Yoon BH, Kim CJ. Chorionic plate vessels as an origin of amniotic fluid neutrophils. Pathol Int 2004; 54: 516-22.
44. Naeye RL. Functionally important disorders of the placenta, umbilical-cord, and fetal membranes. Hum Pathol 1987; 18: 680-691.
45. Steel JH, O'donoghue K, Kennea NL, Sullivan MH, Edwards AD. Maternal origin of inflammatory leukocytes in preterm fetal membranes, shown by fluorescence in situ hybridisation. Placenta 2005; 26: 672-77.
46. Yoon BH, Romero R, Park JS, Kim M, Oh SY, Kim CJ, Jun JK 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: 1124-129.
47. Redline RW, Faye-Petersen O, Heller D. Amniotic infection syndrome: Nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol 2003; 6: 435-48.
48. Sebire NJ. Choriodecidual inflammatory syndrome (CoDIS) is the leading, and under recognised, cause of early preterm delivery and second trimester miscarriage. Med Hypoth 2001; 56: 497-500.
49. Gomez R, Romero R, Ghezzi F, Yoon BH, Mazor M, Berry SM. The fetal inflammatory response syndrome. Am J Obstet Gynecol 1998; 179: 194-202.
50. Lau J, Magee F, Qiu Z, Houb́e J, Von Dadelszen P, Lee SK. Chorioamnionitis with a fetal inflammatory response is associated with higher neonatal mortality, morbidity, and resource use than chorioamnionitis displaying a maternal inflammatory response only.AmJObstet Gynecol 2005; 193: 708-13.
51. Duncombe G, Veldhuizen RA, Gratton RJ, Han VK, Richardson BS. IL-6 and TNF alpha across the umbilical circulation in term pregnancies: Relationship with labour events. Early Hum Dev 2010; 86: 113-17.
52. Lee SE, Romero R, Jung H, Park CW, Park JS, Yoon BH. The intensity of the fetal inflammatory response in intraamniotic inflammation with and without microbial invasion of the amniotic cavity. Am J Obstet Gynecol 2007; 197: 294e1-6.
53. Romero R, Gomez R,Ghezzi F. A fetal systemic inflammatory response is followed by the spontaneous onset of preterm parturition. Am J Obstet Gynecol 1998; 179: 186-93.
54. Royal College of Obstetricians and Gynaecologists. Preterm prelabour rupture of membranes. Guideline No 44. 2006, London: RCOG.
55. Angus SR, Segel SY, Hsu CD, Locksmith GJ, Clark P, Sammel MD, et al. Amniotic fluid matrix metalloproteinase-8 indicates intra-amniotic infection. Am J Obstet Gynecol 2001; 185: 1232-238.
56. Kim KW, Romero R, Park HS, Kim KW, Romero R, Park HS, Park CW, Shim SS, Jun JK, Yoon BH 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.
57. Lee SJ,Won HS, KimMN, Lee PR, Shim JY, Kim A. Diagnostic value of thematrixmetalloproteinase-8 rapid test for detecting microbial invasion of the amniotic cavity. Eur J Clin Microbiol Infect Dis 2008; 27: 1257-260.
58. Park CW, Moon KC, Park JS, Jun JK, Romero R, Yoon BH. 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.
59. Akers A, Jarzembowski JA, Johnson CT, Lieberman RW, Dalton VK. Examining the relationship between positive mid-gestational fetal fibronectin assays and histological evidence of acute placental inflammation. J Perinat Med 2007; 35: 36-42.
60. Al-Adnani M, Sebire NJ. The role of perinatal pathological examination in subclinical infection in obstetrics. Best Pract Res Clin Obstet Gynaecol 2007; 21: 505-21.
61. Wu HC, Shen CM, Wu YY, Yuh YS, Kua KE. Subclinical histologic chorioamnionitis and related clinical and laboratory parameters in preterm deliveries. Pediatr Neonatol 2009; 50: 217-21.
62. Carroll S, Sebire NJ, Nicolaides K. Preterm prelabour amniorrhexis. Parthenon Press, Carnforth, 1996
63. Bruch JF, Bingen E, Fondacci C, et al. The value of chorioamniotic plate smears in predicting intraamniotic infection. Tropho Res 1994; 8: 177-91.
64. Benirschke K, Clifford SH. Intrauterine bacterial infection of the newborn infant: Frozen sections of the cord as an aid to early detection. J Pediatr 1959: 54: 11-18.
65. Mendilcioglu I, Kilicarslan B, Gurkan Zorlu C, Karaveli S, Uner M, Trak B. Placental biopsy by frozen section: Does it have a role in evaluation of fetal well-being? Aust NZ J Obstet Gynecol 2003; 43: 433-37.
66. Sebire NJ. Distribution of histological chorioamnionitis in placental membranes: does a membrane roll provide additional information? J Pathol 2001; 195: 18A.
67. Gersell DJ, PhillipsNJ, Beckerman K. Chronic chorioamnionitis: a clinicopathologic study of 17 cases. Int J Gynecol Pathol 1991; 10: 217-29.
68. Jacques SM, Qureshi F. Chronic chorioamnionitis: a clinicopathologic and immunohistochemical study. Hum Pathol 1998; 29: 1457-61.
69. Kim CJ, Romero R, Kusanovic JP, Yoo W, Dong Z, Topping V, Gotsch F, Yoon BH, Chi JG, Kim JS. The frequency, clinical significance, and pathological features of chronic chorioamnionitis: a lesion associated with spontaneous preterm birth. Mod Pathol 2010; 23: 1000-11.
70. Hecht JL, Fichorova RN, Tang VF, Allred EN, McElrath TF, Leviton A; for the ELGAN study investigators. The relationship between neonatal blood protein profiles and placenta histologic characteristics in extremely low gestation age newborns. Pediatr Res 2011; 69: 68-73.
71. Soper DE, Mayhall CG, Dalton HP. Risk-factors for intraamniotic infection-a prospective epidemiologic-study. Am J Obstet Gynecol 1989; 161: 562-68.
72. Soper DE, Mayhall CG, Froggatt JW. Characterization and control of intraamniotic infection in an urban teaching hospital. Am J Obstet Gynecol 1996; 175: 304-309.
73. Shalak LF, Laptook AR, Jafri HS, Ramilo O, Perlman JM. Clinical chorioamnionitis, elevated cytokines, and brain injury in term infants. Pediatr 2002; 110: 673-80.
74. Soraisham AS, Singhal N, McMillan DD, Sauve RS, Lee SK; Canadian Neonatal Network., A multicenter study on the clinical outcome of chorioamnionitis in preterm infants. Am J Obstet Gynecol 2009; 200: 372.e1-6.
75. Sebire NJ, Goldin RD, Regan L. Histological chorioamnionitis in relation to clinical presentation at 14-40 weeks of gestation. J Obstet Gynecol 2001; 21: 242-45.
76. Guzick DS,Winn K. The association of chorioamnionitiswith pretermdelivery. Obstet Gynecol 1985;65: 11-16.
77. Seong HS, Lee SE, Kang JH, Romero R, Yoon BH. The frequency of microbial invasion of the amniotic cavity and histologic chorioamnionitis in women at term with intact membranes in the presence or absence of labor. Am J Obstet Gynecol. 2008; 199: 375.e1-5.
78. Mi Lee S, Romero R, Lee KA, Jin Yang H, Joon Oh K, Park CW 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.
79. LewisDF, Major CA, Towers CV, Asrat T, Harding JA, Garite TJ. Effects of digital vaginal examinations on latency period in preterm premature rupture of membranes. Obstet Gynecol 1992; 80: 630-34.
80. Smulian JC, Shen-Schwarz S, Vintzileos AM, Lake MF, Ananth CV. Clinical chorioamnionitis and histologic placental inflammation. Obstet Gynecol 1999; 94: 1000-1005.
81. Royal College of Obstetricians and Gynaecologists, Prevention of early onset neonatal group B streptococcal disease. Guideline No 36. 2003, London: RCOG.
82. National Screening Committee. Group B streptoccocus screening. (2008
83. CDC, Provisional recommendations for the prevention of perinatal group B streptococcal disease. 2010, National Center for Immunization and Respiratory Disease, Atlanta, U.S.
84. Goldenberg RL. The management of preterm labor. Obstet Gynecol 2002; 100: 1020-37.
85. Vrachnis N, Vitoratos N, Iliodromiti Z, Sifakis S, Deligeoroglou E, Creatsas G. Intrauterine inflammation and preterm delivery. Ann N York Acad Sci 2010; 1205: 118-22.
86. Mueller-Heubach E, Rubinstein DN, Schwarz SS. Histologic chorioamnionitis and preterm delivery in different patient populations. Obstet Gynecol 1990; 75: 622-26.
87. Goldenberg RL, Hauth JC, Andrews WW. Mechanisms of disease-Intrauterine infection and preterm delivery. New Eng J Med 2000; 342: 1500-507.
88. Zlatnik FJ, Gellhaus TM, Benda JA, Koontz FP, Burmeister LF. Histologic chorioamnionitis, microbial infection, and prematurity. Obstet Gynecol 1990; 76: 355-59.
89. Andrews WW, Hauth JC, Goldenberg RL. Infection and preterm birth. Am J Perinatol 2000; 17: 357-65.
90. Galask RP, Varner MW, Petzold CR, Wilbur SL. Bacterial attachment to the chorioamniotic membranes. Am J Obstet Gynecol 1984; 148: 915-28.
91. Gonźalez-Bosquet E, Cerqueira MJ, Dominguez C, Gasser I, Bermejo B, Cabero L. Amniotic fluid glucose and cytokines values in the early diagnosis of amniotic infection in patients with preterm labor and intact membranes. J Mat Fetal Med 1999; 8: 155-58.
92. Romero R, Yoon BH, Mazor M. 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.
93. Figueroa R, Garry D, Elimian A, Patel K, Sehgal PB, Tejani N. Evaluation of amniotic fluid cytokines in preterm labor and intact membranes. J Mat Fetal Neonat Med 2005; 18: 241-47.
94. Himes KP, Simhan HN. Risk of recurrent preterm birth and placental pathology. Obstet Gynecol 2008; 112: 121-26.
95. Goldenberg RL, Andrews WW, Faye-Petersen O, Cliver S, Goepfert AR, Hauth JC. The Alabama Preterm Birth Project: Placental histology in recurrent spontaneous and indicated preterm birth. Am J Obstet Gynecol 2006; 195: 792-96.
96. Moretti M, Sibai BM. Maternal and perinatal outcome of expectantmanagement of premature rupture of membranes in the midtrimester. Am J Obstet Gynecol 1988; 159: 390-96.
97. Yang LC, Taylor DR, Kaufman HH, Hume R, Calhoun B. Maternal and fetal outcomes of spontaneous preterm premature rupture of membranes. J Am Osteopath Ass 2004; 104: 537-42.
98. Oliveira Neto AF, Parpinelli MA, Cecatti JG, Souza JP, Sousa MH. Factors associated with maternal death in women admitted to an intensive care unit with severe maternal morbidity. Int J Gynecol Obstet 2009; 105: 252-56.
99. Ananth CV, Getahun D, Peltier MR, Smulian JC. Placental abruption in term and preterm gestations: evidence for heterogeneity in clinical pathways. Obstet Gynecol 2006; 107: 785-92.
100. Nath CA, Ananth CV, Smulian JC, Shen-Schwarz S, Kaminsky L. Histologic evidence of inflammation and risk of placental abruption. Am J Obstet Gynecol 2007; 197: 319.e1-6.
101. Rouse DJ, Landon M, Leveno KJ, et al. The Maternal-Fetal Med Units cesarean registry: chorioamnionitis at term and its duration-relationship to outcomes. Am J Obstet Gynecol 2004; 191: 211-6.
102. Lahra MM, Gordon A, Jeffery HE. Chorioamnionitis and fetal response in stillbirth. Am J Obstet Gynecol 2007; 196: 229-30.
103. Moyo SR, Hägerstrand I, Nyström L, et al. Stillbirths and intrauterine infection, histologic chorioamnionitis and microbiological findings. Int J Gynecol Obstet 1996; 54: 115-23.
104. Royal College of Obstetricians and Gynaecologists. Intrauterine infection and perinatal brain injury. Scientific Advisory Committee Opinion Paper 3. 2007, London: RCOG.
105. Costeloe K, Hennessy E, Gibson AT, Marlow N, Wilkinson AR. The EPICure study: outcomes to discharge from hospital for infants born at the threshold of viability. Pediatr 2000; 106: 659-71.
106. Wu YW, Colford JM. Chorioamnionitis as a risk factor for cerebral palsy: A meta-analysis. J AmMed Ass 2000; 284: 1417-424.
107. Wu YW. Systematic review of chorioamnionitis and cerebral palsy. Ment Retard Dev Disabil Res Rev 2002; 8: 25-29.
108. Shatrov JG, Birch SC, Lam LT, Quinlivan JA, McIntyre S, Mendz GL. Chorioamnionitis and cerebral palsy: a meta-analysis. Obstet Gynecol 2010; 116: 387-92.
109. Leviton A, Allred EN, Kuban KC, Hecht JL, Onderdonk AB, O'shea TM et al. Microbiologic and histological characteristics of the extremely preterm infant's placenta predict white matter damage and later cerebral palsy. The ELGAN study. Pediatr Res 2010; 67: 95-101.
110. Maleki Z, Bailis AJ, Argani CH, Askin FB, Graham EM. Periventricular leukomalacia and placental histopathologic abnormalities. Obstet Gynecol 2009; 114: 1115-120.
111. Andrews WW, Goldenberg RL, Faye-Petersen O, Cliver S, Goepfert AR, Hauth JC. 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: 803-808.
112. Zanardo V, Vedovato S, Suppiej A, Trevisanuto D, Migliore M, Di Venosa B et al. Histological inflammatory responses in the placenta and early neonatal brain injury. Pediatr Dev Pathol 2008; 11: 350-54.
113. Redline RW, Minich N, Taylor HG, Hack M. Placental lesions as predictors of cerebral palsy and abnormal neurocognitive function at school age in extremely low birth weight infants
114. Blume HK, Li CI, Loch CM, Koepsell TD. Intrapartum fever and chorioamnionitis as risks for encephalopathy in term newborns: a case control study. Dev Med Child Neurol 2008; 50: 19-24.
115. Abu-Maziad A, Schaa K, Bell EF, Dagle JM, Cooper M, Marazita ML, Murray JC et al. Role of polymorphic variants as genetic modulators of infection in neonatal sepsis. Pediatr Res 2010; 68: 323-29.
116. Botet F, Figueras J, Carbonell-Estrany X, Arca G, The Castrillo Study Group. Effect of maternal clinical chorioamnionitis on neonatal morbidity in very-low birthweight infants: a case-control study. J Perinat Med 2010; 38: 269-73.
117. Klinger G, Levy I, Sirota L, Boyko V, Reichman B, Lerner-Geva L. Israel Neonatal Network. Epidemiology and risk factors for early onset sepsis among very-low-birthweight infants. Am J Obstet Gynecol 2009; 201: 38 e1-6.
118. Madsen-Bouterse SA, Romero R, Tarca AL, Kusanovic JP, Espinoza J, Kim CJ et al. The transcriptome of the fetal inflammatory response syndrome. Am J Reprod Immunol 2010; 63: 73-92.
119. Watterberg KL, Demers LM, Scott SM, Murphy S. Chorioamnionitis and early lung inflammation in infants in whom bronchopulmonary dysplasia develops. Pediatr 1996; 97: 210-15.
120. Lahra MM, Beeby PJ, Jeffery HE. Maternal versus fetal inflammation and respiratory distress syndrome: a 10-year hospital cohort study. Arch Dis Child Fetal Neonat Ed 2009; 94: F13-F16.
121. Been JV, Rours IG, Kornelisse RF, Jonkers F, de Krijger RR, Zimmermann LJ. Chorioamnionitis alters the response to surfactant in preterm infants. J Pediatr 2010; 156: 10-34.
122. Jobe AH, Kallapur SG. Chorioamnionitis, surfactant, and lung disease in very low birth weight infants. J Pediatr 2010; 156: 3-4.
123. Rastogi S, Rastogi D, Sundaram R, Kulpa J, Parekh AJ. Leukemoid reaction in extremely low-birthweight infants. Am J Perinatol 1999; 16: 93-7.
124. Calhoun DA, Kirk JF, Christensen RD. Incidence, significance, and kinetic mechanism responsible for leukemoid reactions in patients in the neonatal intensive care unit: a prospective evaluation. J Pediatr 1996 129: 403-409.
125. Hsiao R, Omar SA. Outcome of extremely low birth weight infants with leukemoid reaction. Pediatr 2005; 116: e43-51.
126. Zanardo V, Vedovato S, Trevisanuto DD. Histological chorioamnionitis and neonatal leukemoid reaction in low-birth-weight infants. Hum Pathol 2006; 37: 87-91.