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HISTOLOGICAL CHORIOAMNIONITIS: CURRENT CONCEPTS OF DIAGNOSIS, CLASSIFICATION AND CLINICAL SIGNIFICANCE

Published online by Cambridge University Press:  04 February 2011

F JESSOP  and
NJ SEBIRE
F JESSOP
Affiliation:
Department of Paediatric Pathology, Addenbrookes Hospital, Cambridge
NJ SEBIRE*
Affiliation:
Department of Paediatric Pathology, Great Ormond Street Hospital, London
*
Professor NJ Sebire, Department of Histopathology, Camelia Botnar Laboratories, Great Ormond Street Hospital, Great Ormond Street, London WC1N 3JH, United Kingdom. Email: sebirn@gosh.nhs.uk
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Extract

Interest in the clinical associations between maternal intrapartum fever and adverse neonatal outcome has been longstanding, with publications of a relationship between maternal fever and cerebral palsy dating from the 1950s. Further recognition of the associations between either clinically or histologically characterised chorioamnionitis, ascending infection and neonatal wellbeing followed, with numerous reports in the 1960s and 70s, particularly as the neonatal significance of group B streptococcal infections became apparent. Similarly, with the systematic introduction of diagnostic light microscopy into clinical medicine, chorioamnionitis (inflammation of the placental membranes) and funisitis (inflammation of the umbilical cord) were recognised as distinct histological entities, with increasing recognition that the aetiology was likely to be infective. There are numerous texts discussing in detail the pathogenesis and histological features of chorioamnionitis and funisitis. The aim of this review is to provide an overview of the salient associated issues for clinical practitioners and to highlight areas of ongoing uncertainty and recent developments in understanding.

Type
Research Article
Information
Fetal and Maternal Medicine Review , Volume 22 , Issue 1 , February 2011 , pp. 25 - 44
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

1Speert, H. Memorable medical mentors: V; Nicholson J Eastman. Obstet Gynecol Surv 2004; 59: 399–405.CrossRefGoogle Scholar
2William, MD, Blanc, P. Pathways of fetal and early neonatal infection: Viral placentitis, bacterial and fungal chorioamnionitis.J Pediatr 1961; 59: 473–96.Google Scholar
3Fox, H, Sebire, NJ. Infections and inflammatory lesions of the placenta. Pathology of the Placenta 2007; Saunders, Elsevier, London, 303–354.CrossRefGoogle Scholar
4Hood, 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.CrossRefGoogle ScholarPubMed
5Benirschke, K, Kaufman, P, Baergen, RN. Pathology of the Human Placenta. 5th ed. 2006, New York: Springer, 657–760.Google Scholar
6Lewis, SH, Perrin, E. Pathology of the Placenta. Churchill Livingstone, New York, 1999Google Scholar
7Bobitt, JR, Ledger, WJ. Amniotic-fluid analysis – its role in maternal and neonatal infection. Obstet Gynecol 1978; 51: 56–62.Google Scholar
8MacVicar, J. Chorioamnionitis. Clin Obstet Gynecol 1970; 13: 272–90.Google Scholar
9Bobitt, JR, Ledger, WJ. Unrecognized amnionitis and prematurity – preliminary-report. J Reprod Med 1977; 19: 8–12.Google Scholar
10White, CA, Longnecker, DS. Leukocytic infiltration of the umbilical cord. Fetal infection or hypoxia? Obstet Gynecol 1967; 29: 711–18.Google ScholarPubMed
11Olding, L. Value of placentitis as a sign of intrauterine infection in human subjects. Acta Pathol Microbiol Scand 1970; 78: 256–64.Google Scholar
12Dominguez, 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.Google Scholar
13Seong, 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.CrossRefGoogle ScholarPubMed
14Pettker, 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.CrossRefGoogle ScholarPubMed
15Satosar, 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.CrossRefGoogle ScholarPubMed
16Srinivas, 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.CrossRefGoogle ScholarPubMed
17Han, 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.Google Scholar
18Jones, 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: e8205CrossRefGoogle ScholarPubMed
19Benirschke, K. What pediatricians should know about the placenta. Current Prob Pediatr 1971; 2: 3–32.Google Scholar
20Robbins, SJ, Kumar, V. Robbins & Cotran Pathologic Basis of Dis, Saunders, New York, 2009.Google Scholar
21Anderson, 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.CrossRefGoogle Scholar
22Murray, PE. Manual of Clinical Microbiology, 8th Ed. 2003, Washington: ASM Press.Google Scholar
23Cassell, 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.Google Scholar
24Larsen, B, Hwang, J. Mycoplasma, ureaplasma, and adverse pregnancy outcomes: a fresh look. Infect Dis Obstet Gynecol 2010; 2010 pii: 521921.CrossRefGoogle ScholarPubMed
25Waites, 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.CrossRefGoogle ScholarPubMed
26Berger, 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.Google Scholar
27Yoon, 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.Google Scholar
28Kirchner, 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.CrossRefGoogle ScholarPubMed
29Jazayeri, 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.Google Scholar
30Han, 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.CrossRefGoogle Scholar
31Khader, 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.Google Scholar
32Jadhav, AR, Belfort, MA, Dildy, GA. Eikenella corrodens chorioamnionitis: modes of infection? Am J Obstet Gynecol 2009; 200: e4–e5.Google Scholar
33Schwartz, 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.Google Scholar
34Altshuler, G. Pathogenesis of congenital herpes virus infection: case report including a description of the placenta. Am J Dis Child 1974; 127: 427–29.CrossRefGoogle ScholarPubMed
35Srinivas, 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. Am J Obstet Gynecol 2006; 195: 797–802.Google Scholar
36Menon, R, Taylor, RN, Fortunato, SJ. Chorioamnionitis; a complex pathophysiologic syndrome. Placenta 2010; 31: 113–20.Google Scholar
37Ma, 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.CrossRefGoogle ScholarPubMed
38Kacerovsky, 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.CrossRefGoogle ScholarPubMed
39Buhimschi, 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.Google Scholar
40Romero, 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.Google Scholar
41Romero, 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.Google Scholar
42Romero, 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.Google Scholar
43Lee, 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.CrossRefGoogle ScholarPubMed
44Naeye, RL. Functionally important disorders of the placenta, umbilical-cord, and fetal membranes. Hum Pathol 1987; 18: 680–691.Google Scholar
45Steel, 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.CrossRefGoogle ScholarPubMed
46Yoon, 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.CrossRefGoogle ScholarPubMed
47Redline, RW, Faye-Petersen, O, Heller, D. Amniotic infection syndrome: Nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol 2003; 6: 435–48.CrossRefGoogle ScholarPubMed
48Sebire, 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.Google Scholar
49Gomez, R, Romero, R, Ghezzi, F, Yoon, BH, Mazor, M, Berry, SM. The fetal inflammatory response syndrome. Am J Obstet Gynecol 1998; 179: 194–202.CrossRefGoogle ScholarPubMed
50Lau, J, Magee, F, Qiu, Z, Houbé, 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. Am J Obstet Gynecol 2005; 193: 708–13.CrossRefGoogle ScholarPubMed
51Duncombe, 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.Google Scholar
52Lee, 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.CrossRefGoogle ScholarPubMed
53Romero, 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.CrossRefGoogle ScholarPubMed
54Royal College of Obstetricians and Gynaecologists. Preterm prelabour rupture of membranes. Guideline No 44. 2006, London: RCOG.Google Scholar
55Angus, 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.Google Scholar
56Kim, 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.CrossRefGoogle ScholarPubMed
57Lee, SJ, Won, HS, Kim, MN, Lee, PR, Shim, JY, Kim, A. Diagnostic value of the matrix metalloproteinase-8 rapid test for detecting microbial invasion of the amniotic cavity. Eur J Clin Microbiol Infect Dis 2008; 27: 1257–260.Google Scholar
58Park, 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.Google Scholar
59Akers, 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.Google Scholar
60Al-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.Google Scholar
61Wu, 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.Google Scholar
62Carroll, S, Sebire, NJ, Nicolaides, K. Preterm prelabour amniorrhexis. Parthenon Press, Carnforth, 1996Google Scholar
63Bruch, JF, Bingen, E, Fondacci, C, et al. The value of chorioamniotic plate smears in predicting intra-amniotic infection. Tropho Res 1994; 8: 177–91.Google Scholar
64Benirschke, 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.Google Scholar
65Mendilcioglu, 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.Google Scholar
66Sebire, NJ. Distribution of histological chorioamnionitis in placental membranes: does a membrane roll provide additional information? J Pathol 2001; 195: 18A.Google Scholar
67Gersell, DJ, Phillips, NJ, Beckerman, K. Chronic chorioamnionitis: a clinicopathologic study of 17 cases. Int J Gynecol Pathol 1991; 10: 217–29.Google Scholar
68Jacques, SM, Qureshi, F. Chronic chorioamnionitis: a clinicopathologic and immunohistochemical study. Hum Pathol 1998; 29: 1457–61.Google Scholar
69Kim, 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.Google Scholar
70Hecht, 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.Google Scholar
71Soper, DE, Mayhall, CG, Dalton, HP. Risk-factors for intraamniotic infection – a prospective epidemiologic-study. Am J Obstet Gynecol 1989; 161: 562–68.CrossRefGoogle ScholarPubMed
72Soper, DE, Mayhall, CG, Froggatt, JW. Characterization and control of intraamniotic infection in an urban teaching hospital. Am J Obstet Gynecol 1996; 175: 304–309.CrossRefGoogle Scholar
73Shalak, LF, Laptook, AR, Jafri, HS, Ramilo, O, Perlman, JM. Clinical chorioamnionitis, elevated cytokines, and brain injury in term infants. Pediatr 2002; 110: 673–80.Google Scholar
74Soraisham, 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.CrossRefGoogle Scholar
75Sebire, 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.Google Scholar
76Guzick, DS, Winn, K. The association of chorioamnionitis with preterm delivery. Obstet Gynecol 1985; 65: 11–16.Google Scholar
77Seong, 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.Google Scholar
78Mi 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.Google Scholar
79Lewis, DF, 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.Google Scholar
80Smulian, JC, Shen-Schwarz, S, Vintzileos, AM, Lake, MF, Ananth, CV. Clinical chorioamnionitis and histologic placental inflammation. Obstet Gynecol 1999; 94: 1000–1005.Google Scholar
81Royal College of Obstetricians and Gynaecologists, Prevention of early onset neonatal group B streptococcal disease. Guideline No 36. 2003, London: RCOG.Google Scholar
82National Screening Committee. Group B streptoccocus screening. (2008)Google Scholar
83CDC, Provisional recommendations for the prevention of perinatal group B streptococcal disease. 2010, National Center for Immunization and Respiratory Disease, Atlanta, US.Google Scholar
84Goldenberg, RL. The management of preterm labor. Obstet Gynecol 2002; 100: 1020–37.Google Scholar
85Vrachnis, 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.Google Scholar
86Mueller-Heubach, E, Rubinstein, DN, Schwarz, SS. Histologic chorioamnionitis and preterm delivery in different patient populations. Obstet Gynecol 1990; 75: 622–26.Google Scholar
87Goldenberg, RL, Hauth, JC, Andrews, WW. Mechanisms of disease – Intrauterine infection and preterm delivery. New Eng J Med 2000; 342: 1500–507.Google Scholar
88Zlatnik, FJ, Gellhaus, TM, Benda, JA, Koontz, FP, Burmeister, LF. Histologic chorioamnionitis, microbial infection, and prematurity. Obstet Gynecol 1990; 76: 355–59.Google Scholar
89Andrews, WW, Hauth, JC, Goldenberg, RL. Infection and preterm birth. Am J Perinatol 2000; 17: 357–65.Google Scholar
90Galask, RP, Varner, MW, Petzold, CR, Wilbur, SL. Bacterial attachment to the chorioamniotic membranes. Am J Obstet Gynecol 1984; 148: 915–28.Google Scholar
91González-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.Google Scholar
92Romero, 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.Google Scholar
93Figueroa, 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.Google Scholar
94Himes, KP, Simhan, HN. Risk of recurrent preterm birth and placental pathology. Obstet Gynecol 2008; 112: 121–26.CrossRefGoogle ScholarPubMed
95Goldenberg, 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.Google Scholar
96Moretti, M, Sibai, BM. Maternal and perinatal outcome of expectant management of premature rupture of membranes in the midtrimester. Am J Obstet Gynecol 1988; 159: 390–96.Google Scholar
97Yang, 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.Google Scholar
98Oliveira 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.CrossRefGoogle Scholar
99Ananth, 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.Google Scholar
100Nath, 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.Google Scholar
101Rouse, 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.Google Scholar
102Lahra, MM, Gordon, A, Jeffery, HE. Chorioamnionitis and fetal response in stillbirth. Am J Obstet Gynecol 2007; 196: 229–30.Google Scholar
103Moyo, SR, Hägerstrand, I, Nyström, L, et al. Stillbirths and intrauterine infection, histologic chorioamnionitis and microbiological findings. Int J Gynecol Obstet 1996; 54: 115–23.Google Scholar
104Royal College of Obstetricians and Gynaecologists. Intrauterine infection and perinatal brain injury. Scientific Advisory Committee Opinion Paper 3. 2007, London: RCOG.Google Scholar
105Costeloe, 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.Google Scholar
106Wu, YW, Colford, JM. Chorioamnionitis as a risk factor for cerebral palsy: A meta-analysis. J Am Med Ass 2000; 284: 1417–424.CrossRefGoogle ScholarPubMed
107Wu, YW. Systematic review of chorioamnionitis and cerebral palsy. Ment Retard Dev Disabil Res Rev 2002; 8: 25–29.Google Scholar
108Shatrov, JG, Birch, SC, Lam, LT, Quinlivan, JA, McIntyre, S, Mendz, GL. Chorioamnionitis and cerebral palsy: a meta-analysis. Obstet Gynecol 2010; 116: 387–92.Google Scholar
109Leviton, 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.Google Scholar
110Maleki, Z, Bailis, AJ, Argani, CH, Askin, FB, Graham, EM. Periventricular leukomalacia and placental histopathologic abnormalities. Obstet Gynecol 2009; 114: 1115–120.Google Scholar
111Andrews, 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.Google Scholar
112Zanardo, 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.Google Scholar
113Redline, 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 (<1kg). Pediatr Dev Pathol 2007; 10: 282–92.Google Scholar
114Blume, 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.Google Scholar
115Abu-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.Google Scholar
116Botet, 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.Google Scholar
117Klinger, 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.Google Scholar
118Madsen-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.Google Scholar
119Watterberg, KL, Demers, LM, Scott, SM, Murphy, S. Chorioamnionitis and early lung inflammation in infants in whom bronchopulmonary dysplasia develops. Pediatr 1996; 97: 210–15.Google Scholar
120Lahra, 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.Google Scholar
121Been, 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.Google Scholar
122Jobe, AH, Kallapur, SG. Chorioamnionitis, surfactant, and lung disease in very low birth weight infants. J Pediatr 2010; 156: 3–4.Google Scholar
123Rastogi, S, Rastogi, D, Sundaram, R, Kulpa, J, Parekh, AJ. Leukemoid reaction in extremely low-birth-weight infants. Am J Perinatol 1999; 16: 93–7.Google Scholar
124Calhoun, 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.CrossRefGoogle ScholarPubMed
125Hsiao, R, Omar, SA. Outcome of extremely low birth weight infants with leukemoid reaction. Pediatr 2005; 116: e43–51.Google Scholar
126Zanardo, V, Vedovato, S, Trevisanuto, DD. Histological chorioamnionitis and neonatal leukemoid reaction in low-birth-weight infants. Hum Pathol 2006; 37: 87–91.Google Scholar