Chorioamnionitis: diagnosis and role in complications during pregnancy and fetal development

1. Петровский Б.В., гл. ред. Энциклопедический словарь медицинских терминов: в 3-х томах. М.: Советская энциклопедия; 1984: т. 3: 261. [Gl. ed. by B.V. Petrovsky. Encyclopedic dictionary of medical terms: in 3 volumes. Moscow: Soviet Encyclopedia; 1984: vol. 3: 261. (in Russian).]
2. Redline R.W. Placental inflammation. Semin. Neonatol. 2004; 9(4): 265-74. https://dx.doi.org/ 10.1016/j.siny.2003.09.005.
3. Romero R., Kim Y.M., Pacora P., Kim C.J., Benshalom-Tirosh N., Jaiman S. et al. The frequency and type of placental histologic lesions in term pregnancies with normal outcome. J. Perinat. Med. 2018; 46(6): 613-30. https://dx.doi.org/10.1515/jpm-2018-0055.
4. Международная статистическая классификация болезней и проблем, связанных со здоровьем; 10-й пересмотр. Женева: ВОЗ; 2003: т. 1, ч. 2. 633 с. [International Statistical Classification of Diseases and Health-related Problems; 10th revision. Geneva: WHO; 2003: vol. 1, pt 2. 633 p. (in Russian)].
5. World Health Organization. WHO recommendations for prevention and treatment of maternal peripartum infections. Geneva: WHO; 2015.
6. Committee Opinion No. 712: Intrapartum management of intraamniotic infection. Obstet. Gynecol. 2017; 130(2): e95-e101. https://dx.doi.org/10.1097/AOG.0000000000002236.
7. Министерство здравоохранения Российской Федерации. Инфекции амниотической полости и плодных оболочек (хориамнионит). Клинические рекомендации; 2023. 48 с. [Ministry of Health of the Russian Federation. Infections of the amniotic cavity and fetal membranes (chorioamnionitis). Clinical guidelines; 2023. 48 p. (in Russian).]
8. Fahey J.O. Clinical management of intra-amniotic infection and chorioamnionitis: a review of the literature. J. Midwifery Womens Health. 2008; 53(3): 227-35. https://dx.doi.org/10.1016/j.jmwh.2008.01.001.
9. Park C.W., Moon K.C., Park J.S., Jun J.K., Romero R., Yoon B.H. 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(1): 56-61. https://dx.doi.org/10.1016/j.placenta.2008.09.017.
10. Waites K.B., Katz B., Schelonka R.L. Mycoplasmas and ureaplasmas as neonatal pathogens. Clin. Microbiol. Rev. 2005; 18(4): 757-89. https://dx.doi.org/10.1128/CMR.18.4.757-789.2005.
11. Conti N., Torricelli M., Voltolini C., Vannuccini S., Clifton V.L., Bloise E. et al. Term histologic chorioamnionitis: a heterogeneous condition. Eur. J. Obstet. Gynecol. Reprod. Biol. 2015; 188: 34-8. https://dx.doi.org/10.1016/j.ejogrb.2015.02.034.
12. Lee Y.H., Shynlova O., Lye S.J. Stretch-induced human myometrial cytokines enhance 466 immune cell recruitment via endothelial activation. Cell. Mol. Immunol. 2015; 12(2): 231-42. https://dx.doi.org/10.1038/cmi.2014.39.
13. Roberts D.J., Celi A.C., Riley L.E., Onderdonk A.B., Boyd T.K., Johnson L.C. et al. Acute histologic chorioamnionitis at term: nearly always noninfectious. PLoS One. 2012; 7(3): e31819. https://dx.doi.org/10.1371/journal.pone.0031819.
14. Щеголев А.И., Серов В.Н. Клиническая значимость поражений плаценты. Акушерство и гинекология. 2019; 3: 54-62. [Shchegolev A.I., Serov V.N. Clinical significance of placental lesions. Obstetrics and Gynecology. 2019; (3): 54-62. (in Russian)]. https://dx.doi.org/10.18565/aig.2019.3.54-62.
15. Anders A.P., Gaddy J.A., Doster R.S., Aronoff D.M. Current concepts in maternal-fetal immunology: Recognition and response to microbial pathogens by decidual stromal cells. Am. J. Reprod. Immunol. 2017; 77(3): e12623. https://dx.doi.org/10.1111/aji.12623.
16. Xu P., Alfaidy N., Challis J.R. Expression of matrix metalloproteinase (MMP)-2 454 and MMP-9 in human placenta and fetal membranes in relation to preterm 455 and term labor. J. Clin. Endocrinol. Metab. 2002; 87(3): 1353-61. https://dx.doi.org/10.1210/jcem.87.3.8320 .
17. Romero R., Miranda J., Chaemsaithong P., Chaiworapongsa T., Kusanovic J.P., Dong Z. et al. Sterile and microbial-associated intra-amniotic inflammation in preterm prelabor rupture of membranes. J. Matern. Fetal Neonatal Med. 2015; 28(12): 1394-409. https://dx.doi.org/10.3109/14767058.2014.958463.
18. Romero R., Miranda J., Chaiworapongsa T., Korzeniewski S.J., Chaemsaithong P., Gotsch F. 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(5): 458-74. https://dx.doi.org/10.1111/aji.12296.
19. Chowdhury B., David A.L., Thrasivoulou C., Becker D.L., Bader D.L., Chowdhury T.T. Tensile strain increased COX-2 expression and PGE2 release leading to weakening of the human amniotic membrane. Placenta. 2014; 35(12): 1057-64. https://dx.doi.org/10.1016/j.placenta.2014.09.006.
20. Kim D.W., Young S.L., Grattan D.R., Jasoni C.L. Obesity during pregnancy disrupts placental morphology, cell proliferation, and inflammation in a sex-specific manner across gestation in the mouse. Biol. Reprod. 2014; 90(6): 130. https://dx.doi.org/10.1095/biolreprod.113.117259.
21. Dubova E.A., Pavlov K.A., Shchegolev A.I., Borovkova E.I., Bayramova M.A., Makarov I.O. Vascular endothelial growth factor and its receptors in the placenta of pregnant women with obesity. Bull. Exp. Biol. Med. 2011; 151(2): 253-8. https://dx.doi.org/10.1007/s10517-011-1302-3.
22. Jim B., Karumanchi S.A. Preeclampsia: pathogenesis, prevention, and long-term complications. Semin. Nephrol. 2017; 37(4): 386-97. https://dx.doi.org/10.1016/j.semnephrol.2017.05.011.
23. Макаров И.О., Боровикова Е.И., Байрамова М.А., Рыкунова О.В., Дубова Е.А., Павлов К.А., Щеголев А.И. Особенности течения III триместра беременности и родов у пациенток с ожирением. Акушерство и гинекология. 2011; 8: 48-53. [Makarov I.O., Borovikova E.I., Bairamova M.A., Rykunova O.V., Dubova E.A., Pavlov K.A., Shchegolev A.I. The specific features of the third trimester of pregnancy and labor in obese patients. Obstetrics and Gynecology. 2011; (8): 48-53. (in Russian)].
24. Gibbs R.S., Blanco J.D. Premature rupture of the membranes. Obstet. Gynecol. 1982; 60(6): 671-9.
25. Carter S.W.D., Neubronner S., Su L.L., Dashraath P., Mattar C., Illanes S.E. et al. Chorioamnionitis: an update on diagnostic evaluation. Biomedicines. 2023; 11(11): 2922. https://dx.doi.org/10.3390/biomedicines11112922.
26. Lee S.M., Park K.H., Jung E.Y., Kook S.Y., Park H., Jeon S.J. Inflammatory proteins in maternal plasma, cervicovaginal and amniotic fluids as predictors of intra-amniotic infection in preterm premature rupture of membranes. PLoS One. 2018; 13(7): e0200311. https://dx.doi.org/10.1371/journal.pone.0200311.
27. Lisonkova S., Sabr Y., Joseph K. Diagnosis of subclinical amniotic fluid infection prior to rescue cerclage using gram stain and glucose tests: an individual patient meta-analysis. J. Obstet. Gynaecol. Can. 2014; 36(2): 116-22. https://dx.doi.org/10.1016/S1701-2163(15)30656-3.
28. Romero R., Yoon B.H., Kenney J.S., Gomez R., Allison A.C., Sehgal P.B. Amniotic fluid interleukin-6 determinations are of diagnostic and prognostic value in preterm labor. Am. J. Reprod. Immunol. 1993; 30(2-3): 167-83. https://dx.doi.org/10.1111/j.1600-0897.1993.tb00618.x.
29. Park H.S., Kim S.A. 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 (1, Suppl. 1): S174. https://dx.doi.org/10.1016/j.ajog.2014.10.368.
30. Riggs J.W., Blanco J.D. Pathophysiology, diagnosis, and management of intraamniotic infection. In: Seminars in Perinatology. Elsevier: Amsterdam, The Netherlands; 1998.
31. Menon R., Taylor R.N., Fortunato S.J. Chorioamnionitis – a complex pathophysiologic syndrome. Placenta. 2010; 31(2): 113-20. https://dx.doi.org/10.1016/j.placenta.2009.11.012.
32. Щеголев А.И., Дубова Е.А., Павлов К.А. Морфология плаценты. М.; 2010. 46 с. [Shchegolev A.I., Dubova E.A., Pavlov K.A. Morphology of the placenta. Moscow; 2010. 46 p. (in Russian)].
33. Blanc W. Pathology of the placenta and cord in ascending and hematogenous infections In: Marshall W., ed. Perinatal Infections, CIBA Foundation Symposium 77. London: Excerpta Medica; 1980: 17-38.
34. Redline R.W., Faye-Petersen O., Heller D., Qureshi F., Savell V., Vogler C. et al. Amniotic infection syndrome: nosology and reproducibility of placental reaction patterns. Pediatr. Dev. Pathol. 2003; 6(5): 435-48. https://dx.doi.org/10.1007/s10024-003-7070-y.
35. Redline R.W. Classification of placental lesions. Am. J. Obstet. Gynecol. 2015; 213(4, Suppl.): S21-8. https://dx.doi.org/10.1016/j.ajog.2015.05.056.
36. Щеголев А.И. Современная морфологическая классификация повреждений плаценты. Акушерство и гинекология. 2016; 4: 16-23. [Shchegolev A.I. Current morphological classification of damages to the placenta. Obstetrics and Gynecology. 2016; (4): 16-23. (in Russian)]. https://dx.doi.org/10.18565/aig.2016.4.16-23.
37. Higgins R.D., Saade G., Polin R.A., Grobman W.A., Buhimschi I.A., Watterberg K. et al. Chorioamnionitis workshop participants. Evaluation and management of women and newborns with a maternal diagnosis of chorioamnionitis: Summary of a workshop. Obstet. Gynecol. 2016; 127(3): 426-36. https://dx.doi.org/10.1097/AOG.0000000000001246.
38. Romero R., Sepulveda W., Baumann P. The preterm labor syndrome: biochemical, cytologic, immunologic, pathologic, microbiologic, and clinical evidence that preterm labor is a heterogeneous disease. Am. J. Obstet. Gynecol. 1993; 168: 288.
39. Tita A.T., Andrews W.W. Diagnosis and management of clinical chorioamnionitis. Clin. Perinatol. 2010; 37(2): 339-54. https://dx.doi.org/10.1016/j.clp.2010.02.003.
40. Blencowe H., Cousens S., Chou D., Oestergaard M., Say L., Moller A.B. et al. Born too soon: the global epidemiology of 15 million preterm births. Reprod. Health. 2013; 10(Suppl. 1): S2. https://dx.doi.org/10.1186/1742-4755-10-S1-S2.
41. Martinelli P., Sarno L., Maruotti G.M., Paludetto R. Chorioamnionitis and prematurity: a critical review. J. Matern. Fetal Neonatal Med. 2012;25(Suppl. 4): 29-31. https://dx.doi.org/10.3109/14767058.2012.714981.
42. Al-Ostad G., Kezouh A., Spence A.R., Abenhaim H.A. Incidence and risk factors of sepsis mortality in labor, delivery and after birth: population-based study in the USA. J. Obstet. Gynaecol. Res. 2015; 41(8): 1201-6. https://dx.doi.org/110.1111/jog.12710.
43. Милованов А.П., Миханошина Н.А., Лебеденко Е.Ю. Клинико-морфологическая дифференциация сепсиса во время родов и в послеродовом периоде. Доктор.Ру. 2018; 6: 11-6. [Milovanov A.P., Mikhanoshina N.A., Lebedenko E.Yu. Clinical and Morphological Differential diagnosis of sepsis in labor and postpartum. Doctor.Ru. 2018; (6): 11-6. (in Russian)].
44. Garite T.J., Freeman R.K. Chorioamnionitis in the preterm gestation. Obstet. Gynecol. 1982; 59(5): 539-45.
45. Ocheke A.N., Ocheke I.E., Agaba P.A., Imadde G.E., Silas O.A., Ajetunmobi O.I. et al. Maternal and neonatal outcomes of histological chorioamnionitis. J. West Afr. Coll. Surg. 2016; 6(3): 1-14.
46. Ge Y., Zhang C., Cai Y., Huang H. Adverse maternal and neonatal outcomes in women with elevated intrapartum temperature complicated by histological chorioamnionitis at term: A propensity-score matched study. Front. Pediatr. 2021; 9: 654596. https://dx.doi.org/10.3389/fped.2021.654596.
47. Rouse D.J., Landon M., Leveno K.J., Leindecker S., Varner M.W., Caritis S.N. et al. The Maternal-Fetal Medicine Units cesarean registry: chorioamnionitis at term and its duration-relationship to outcomes. Am. J. Obstet. Gynecol. 2004; 191(1): 211-6. https://dx.doi.org/10.1016/j.ajog.2004.03.003.
48. Galletta M.A.K., Schultz R., Sartorelli M.F.G.O.P., Guerra E.C.L., Agra I.K.R., Peres S.V. et al. Clinical characteristics, complications, and predictive model of histological chorioamnionitis in women with preterm premature rupture of membranes. PLoS One. 2023; 18(4): e0283974. https://dx.doi.org/10.1371/journal.pone.0283974.
49. Beck C., Gallagher K., Taylor L.A., Goldstein J.A., Mithal L.B., Gernand A.D. Chorioamnionitis and risk for maternal and neonatal sepsis: a systematic review and meta-analysis. Obstet. Gynecol. 2021; 137(6): 1007-22. https://dx.doi.org/10.1097/AOG.0000000000004377.
50. Liu L.C., Wang Y.C., Yu M.H., Su H.Y. Major risk factors for stillbirth in different trimesters of pregnancy - a systematic review. Taiwan. J. Obstet. Gynecol. 2014; 53(2): 141-5. https://dx.doi.org/10.1016/j.tjog.2014.04.003.
51. Soraisham A.S., Singhal N., McMillan D.D., Sauve R.S., Lee S.K.; Canadian Neonatal Network. A multicenter study on the clinical outcome of chorioamnionitis in preterm infants. Am. J. Obstet. Gynecol. 2009; 200(4): 372.e1-6. https://dx.doi.org/10.1016/j.ajog.2008.11.034.
52. Туманова У.Н., Щеголев А.И. Поражения плаценты в генезе мертворождения (обзор литературы). Международный журнал прикладных и фундаментальных исследований. 2017; 3-1: 77-81. [Tumanova U.N.1, Shchegolev A.I. Placental lesions as the cause of stillbirth (review). International Journal of Applied and Fundamental Research. 2017; (3-1): 77-81. (in Russian)]. https://dx.doi.org/10.17513/mjpfi.11403.
53. Щеголев А.И., Туманова У.Н., Шувалова М.П. Роль хориоамнионита в генезе мертворождения. Международный журнал прикладных и фундаментальных исследований. 2017; 2-2: 205-9. [Shchegolev A.I., Tumanova U.N., Shuvalova M.P. The role of chorioamnionitis at the cause of stillbirth. International Journal of Applied and Fundamental Research. (2-2): 205-9. (in Russian).]
54. Щеголев А.И., Павлов К.А., Дубова Е.А., Фролова О.Г. Ранняя неонатальная смертность в Российской Федерации в 2010 г. Архив патологии. 2013; 75(4): 15-9. [Shchegolev A.I., Pavlov K.A., Dubova E.A., Frolova O.G. Early neonatal mortality in the Russian Federation in 2010. Arkhiv Patologii. 2013; 75(4): 15-9. (in Russian)].
55. Туманова У.Н., Шувалова М.П., Щеголев А.И. Хориоамнионит и ранняя неонатальная смертность (по данным Росстата в 2012–2016 годах). Международный журнал прикладных и фундаментальных исследований. 2018; 8: 49-53. [Tumanova U.N., Shuvalova M.P., Shchegolev A.I. Chorioamnionitis and early neonatal mortality (according to Rosstat in 2012-2016). International Journal of Applied and Fundamental Research. 2018; (8): 49-53. (in Russian)]. https://dx.doi.org/10.17513/mjpfi.12363.
56. Wortham J.M., Hansen N.I., Schrag S.J., Hale E., Van Meurs K., Sánchez P.J. et al. Chorioamnionitis and culture-confirmed, early-onset neonatal infections. Pediatrics. 2016; 137(1): e20152323. https://dx.doi.org/10.1542/peds.2015-2323.
57. Щеголев А.И., Мишнёв О.Д., Туманова У.Н., Шувалова М.П. Неонатальный сепсис как причина перинатальной смертности в Российской Федерации. Международный журнал прикладных и фундаментальных исследований. 2016; 5-4: 589-94. [Shchegolev A.I., Mishnev O.D., Tumanova U.N., Shuvalova M.P. Neonatal sepsis as a cause of perinatal mortality in the Russian Federation. International Journal of Applied and Fundamental Research. 2016; (5-4): 589-94. (in Russian).] https://dx.doi.org/10.17513/mjpfi.9456.
58. Щеголев А.И., Туманова У.Н., Шувалова М.П., Фролова О.Г. Врожденная пневмония как причина перинатальной смертности в Российской Федерации. Неонатология: новости, мнения, обучение. 2016; 2(12): 61-6. [Shchegolev A.I., Tumanova U.N., Shuvalova M.P., Frolova O.G. Congenital pneumonia as a cause of perinatal mortality in the Russian Federation. Neonatology: News, Opinions, Training. 2016; 2(12): 61-6. (in Russian)].
59. Been J.V., Lievense S., Zimmermann L.J., Kramer B.W., Wolfs T.G. Chorioamnionitis as a risk factor for necrotizing enterocolitis: a systematic review and meta-analysis. J. Pediatr. 2013; 162(2): 236-42.e2. https://dx.doi.org/10.1016/j.jpeds.2012.07.012.
60. Garzoni L., Faure C., Frasch M. Fetal cholinergic anti-inflammatory pathway and necrotizing enterocolitis: The brain-gut connection begins in utero. Front. Integr. Neurosci. 2013; 7: 57. https://dx.doi.org/10.3389/fnint.2013.00057.
61. Villamor-Martinez E., Álvarez-Fuente M., Ghazi A.M.T., Degraeuwe P., Zimmermann L.J.I., Kramer B.W. et al. Association of chorioamnionitis with bronchopulmonary dysplasia among preterm infants: a systematic review, meta-analysis, and metaregression. JAMA Netw. Open. 2019; 2(11): e1914611. https://dx.doi.org/10.1001/jamanetworkopen.2019.14611.
62. Yoon B.H., Romero R., Kim K.S., Park J.S., Ki S.H., Kim B.I. et al. A systemic fetal inflammatory response and the development of bronchopulmonary dysplasia. Am. J. Obstet. Gynecol. 1999; 181(4): 773-9. https://dx.doi.org/10.1016/s0002-9378(99)70299-1.
63. Goldenberg R.L., Andrews W.W., Goepfert A.R., Faye-Petersen O., Cliver S.P., Carlo W.A. et al. The Alabama Preterm Birth Study: umbilical cord blood Ureaplasma urealyticum and Mycoplasma hominis cultures in very preterm newborn infants. Am. J. Obstet. Gynecol. 2008; 198(1): 43.e1-5. https://dx.doi.org/10.1016/j.ajog.2007.07.033.
64. Laughon M.M., Langer J.C., Bose C.L., Smith P.B., Ambalavanan N., Kennedy K.A. et al. Prediction of bronchopulmonary dysplasia by postnatal age in extremely premature infants. Am. J. Respir. Crit. Care Med. 2011; 183(12): 1715-22. https://dx.doi.org/10.1164/rccm.201101-0055OC.
65. Jobe A.H. Effects of chorioamnionitis on the fetal lung. Clin. Perinatol. 2012; 39(3): 441-57. https://dx.doi.org/10.1016/j.clp.2012.06.010.
66. Щеголев А.И., Туманова У.Н., Серов В.Н. Роль плаценты в развитии поражений головного мозга новорожденного. Акушерство и гинекология. 2023; 8: 38-47. [Shchegolev A.I., Tumanova U.N., Serov V.N. The role of the placenta in the development of neonatal brain lesions. Obstetrics and Gynecology. 2023; (8): 38-47. (in Russian)]. https://dx.doi.org/10.18568/aig.2023.185.
67. Gantert M., Been J.V., Gavilanes A.W., Garnier Y., Zimmermann L.J., Kramer B.W. Chorioamnionitis: a multiorgan disease of the fetus? J. Perinatol. 2010; 30(Suppl): S21-30. https://dx.doi.org/10.1038/jp.2010.96.
68. Кравченко Е.Н., Куклина Л.В., Баранов И.И. Хориоамнионит. Современный взгляд на проблему. Доктор.Ру. 2022; 21(5): 38-42. [Kravchenko E.N., Kuklina L.V., Baranov I.I. Chorioamnionitis. Modern view of the problem. Doctor.Ru. 2022; 21(5): 38-42. (in Russian).] https://dx.doi.org/10.31550/1727-2378-2022-21-5-38-42.

Received 10.01.2024

Accepted 02.02.2024