Newborn

Register      Login

VOLUME 1 , ISSUE 1 ( January-March, 2022 ) > List of Articles

REVIEW ARTICLE

The Potential Role of Maternal Periodontitis on Preterm Birth and Adverse Neonatal Neurologic Outcomes

Gregory Charles Valentine, Sandra E Juul

Keywords : Inflammation, Neurologic impairment, Periodontitis, Preterm birth

Citation Information : Valentine GC, Juul SE. The Potential Role of Maternal Periodontitis on Preterm Birth and Adverse Neonatal Neurologic Outcomes. 2022; 1 (1):81-90.

DOI: 10.5005/jp-journals-11002-0008

License: CC BY-NC 4.0

Published Online: 31-03-2022

Copyright Statement:  Copyright © 2022; The Author(s).


Abstract

Periodontitis is an often overlooked but important risk factor for both preterm birth and adverse neonatal outcomes. With preterm birth being the leading cause of mortality for all children under the age of 5, any potentially modifiable risk factor associated with preterm birth must be fully evaluated. Periodontal disease is due to bacterial infection of the gingivae with resulting localized and systemic inflammation that can have profound effects in both nonpregnant and pregnant individuals. In pregnancy, several studies have demonstrated an association between periodontitis and preterm birth. Furthermore, extensive evidence demonstrates that fetal exposure to systemic inflammation during gestation predisposes to brain injury and neurodevelopmental delay. Thus, periodontitis and the resulting inflammatory cascade not only affect the pregnant individual but also have significant lifelong consequences on the development and well-being of future offspring. In this review, we will first discuss the epidemiology, prevalence, and pathophysiology of periodontitis. We will then explore the medical literature evaluating the association between periodontitis and preterm birth prior to delving into the potential for neurodevelopmental delay and brain injury among offspring. Finally, we will conclude by discussing future directions and unanswered questions related to periodontitis and its relationship with preterm birth and adverse neonatal outcomes.


HTML PDF Share
  1. Liu L, Oza S, Hogan D, et al. Global, regional, and national causes of child mortality in 2000-13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet 2015;385(9966): 430–440. DOI: 10.1016/S0140-6736(14)61698-6.
  2. Walani SR. Global burden of preterm birth. Int J Gynecol Obstet 2020;150(1):31–33. DOI: 10.1002/ijgo.13195.
  3. Friedrich MJ. Premature birth complications top cause of death in children younger than 5 years. Journal of the American Medical Association 2015;313(3):235. DOI: 10.1001/jama.2014.18326.
  4. Offenbacher S, Beck J, Lieff S, et al. Role of periodontitis in systemic health: spontaneous preterm birth. J Dent Educ 1998;62:852–858. DOI: 10.1002/j.0022-0337.1998.62.10.tb03252.x.
  5. Xiong X, Buekens P, Fraser WD, et al. Periodontal disease and adverse pregnancy outcomes: a systematic review. British journal of obstetrics and gynaecology 2006;113(2):135–143. DOI: 10.1111/j.1471-0528.2005.00827.x.
  6. Offenbacher S, Boggess KA, Murtha AP, et al. Progressive periodontal disease and risk of very preterm delivery. Obstet Gynecol 2006;107(1):29–36. DOI: 10.1097/01.AOG.0000190212.87012.96.
  7. Boggess KA, Lieff S, Murtha AP, et al. Maternal periodontal disease is associated with an increased risk for preeclampsia. Obstet Gynecol 2003;101(2):227–231. DOI: 10.1016/S0029-7844(02)02314-1.
  8. Madianos PN, Bobetsis YA, Offenbacher S. Adverse pregnancy outcomes (APOs) and periodontal disease: pathogenic mechanisms. J Clin Periodontol 2013;40 (Suppl 14):S170–S180. DOI: 10.1111/jcpe.12082.
  9. Arce RM, Barros SP, Wacker B, et al. Increased TLR4 expression in murine placentas after oral infection with periodontal pathogens. Placenta 2009;30(2):156–162. DOI: 10.1016/j.placenta.2008.11.017.
  10. Al-Haddad BJS, Jacobsson B, Chabra S, et al. Long-term risk of neuropsychiatric disease after exposure to infection in utero. JAMA Psychiatry 2019;76(6):594–602. DOI: 10.1001/jamapsychiatry.2019.0029.
  11. Hagberg H, Mallard C, Ferriero DM, et al. The role of inflammation in perinatal brain injury. Nat Rev Neurol 2015;11(4):192–208. DOI: 10.1038/nrneurol.2015.13.
  12. Hagberg H, Gressens P, Mallard C. Inflammation during fetal and neonatal life: implications for neurologic and neuropsychiatric disease in children and adults. Ann Neurol 2012;71(4):444–457. DOI: 10.1002/ana.22620.
  13. Mallard C, Welin AK, Peebles D, et al. White matter injury following systemic endotoxemia or asphyxia in the fetal sheep. Neurochem Res 2003;28(2):215–223. DOI: 10.1023/A:1022368915400.
  14. Kassebaum NJ, Bernabé E, Dahiya M, et al. Global burden of severe periodontitis in 1990-2010: a systematic review and meta-regression. J Dent Res 2014;93(11):1045–1053. DOI: 10.1177/0022034514552491.
  15. Helmi MF, Huang H, Goodson JM, et al. Prevalence of periodontitis and alveolar bone loss in a patient population at Harvard School of Dental Medicine. BMC Oral Health 2019;19(1):254. DOI: 10.1186/s12903-019-0925-z.
  16. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005;366(9499):1809–1820. DOI: 10.1016/S0140-6736(05)67728-8.
  17. Antony KM, Kazembe PN, Pace RM, et al. Population-based estimation of dental caries and periodontal disease rates of gravid and recently postpartum women in Lilongwe, Malawi. AJP Rep 2019;9(3):e268–e274. DOI: 10.1055/s-0039-1695003.
  18. Vogt M, Sallum AW, Cecatti JG, et al. Factors associated with the prevalence of periodontal disease in low-risk pregnant women. Reprod Health 2012;9:3. DOI: 10.1186/1742-4755-9-3.
  19. Nuamah I, Annan BDRT. Periodontal status and oral hygiene practices of pregnant and non-pregnant women. East Afr Med J 1998;75(12):712. PMID: 10065212.
  20. Rakchanok N, Amporn D, Yoshida Y, et al. Dental caries and gingivitis among pregnant and non-pregnant women in Chiang Mai, Thailand. Nagoya J Med Sci 2010;72(1–2):43–50. DOI: 10.18999/nagjms.72.1-2.43.
  21. Borrell LN, Papapanou PN. Analytical epidemiology of periodontitis. J Clin Periodontol 2005;32:132–158. DOI: 10.1111/j.1600-051X.2005.00799.x.
  22. Petersen PE, Bourgeois D, Ogawa H, et al. The global burden of oral diseases and risks to oral health policy and practice the global burden of oral diseases and risks to oral health. Bull World Health Organ 2005;83(9):661–669. PMID: 16211157.
  23. Chapple ILC, Genco R. Diabetes and periodontal diseases: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Clin Periodontol 2013;40:s14:S106. DOI: 10.1111/jcpe.12077.
  24. Tonetti MS, Van Dyke TE. Periodontitis and atherosclerotic cardiovascular disease: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Clin Periodontol 2013;40 (Suppl 14):S24–S29. DOI: 10.1111/jcpe.12089.
  25. Sharma P, Dietrich T, Ferro CJ, et al. Association between periodontitis and mortality in stages 3-5 chronic kidney disease: NHANES III and linked mortality study. J Clin Periodontol 2016;43(2):104–113. DOI: 10.1111/jcpe.12502.
  26. Linden GJ, Lyons A, Scannapieco FA. Periodontal systemic associations: review of the evidence. J Clin Periodontol 2013;40 Suppl 14:S8–S19. DOI: 10.1111/jcpe.12064.
  27. Hillman JD, Socransky SS, Shivers M. The relationships between streptococcal species and periodontopathic bacteria in human dental plaque. Arch Oral Biol 1985;30(11-12):791–795. DOI: 10.1016/0003-9969(85)90133-5.
  28. Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol 2012;10(10):717–725. DOI: 10.1038/nrmicro2873.
  29. Marsh PD. Dental plaque as a biofilm and a microbial community – implications for health and disease. BMC Oral Health 2006;6:S14. DOI: 10.1186/1472-6831-6-S1-S14.
  30. Jenkinson HF, Lamont RJ. Oral microbial communities in sickness and in health. Trends Microbiol 2005;13(12):589–595. DOI: 10.1016/j.tim.2005.09.006.
  31. Socransky SS, Gibbons RJ, Dale AC, et al. The microbiota of the gingival crevice area of man-I. Total microscopic and viable counts and counts of specific organisms. Arch Oral Biol 1963;8:275–280. DOI: 10.1016/0003-9969(63)90019-0.
  32. Socransky SS, Haffajee AD, Cugini MA, et al. Microbial complexes in subgingival plaque. J Clin Periodontol 1998;25(2):134–144. DOI: 10.1111/j.1600-051X.1998.tb02419.x.
  33. Silva N, Abusleme L, Bravo D, et al. Host response mechanisms in periodontal diseases. J Appl Oral Sci 2015;23(3):329–355. DOI: 10.1590/1678-775720140259.
  34. Hajishengallis G, Lambris JD. Microbial manipulation of receptor crosstalk in innate immunity. Nat Rev Immunol 2011;11(3):187–200. DOI: 10.1038/nri2918.
  35. Loe H, Theilade E, Jensen SB. Experimental gingivitis in man. J Periodontol 1965;36:177–187. DOI: 10.1902/jop.1965.36.3.177.
  36. Theilade E, Wright WH, Jensen SB, et al. Experimental gingivitis in man. J Periodontal Res 1966;1:1–13. DOI: 10.1111/j.1600-0765.1966.tb01842.x.
  37. Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal disease: a summary of current work. Lab Investig 1976;34(3):235–249. PMID: 765622.
  38. Anwar N, Zaman N, Nimmi N, et al. Factors associated with periodontal disease in pregnant diabetic women. Mymensingh Med J 2016;25(2):289–295. PMID: 27277362.
  39. Löe H, Silness J. Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontol Scand 1963;21:533–551. DOI: 10.3109/00016356309011240.
  40. Hugoson A. Gingivitis in pregnant women. A longitudinal clinical study. Odontol Revy 1971;22(1):65. PMID: 5280517.
  41. Kornman KS, Loesche WJ. The subgingival microbial flora during pregnancy. J Periodontal Res 1980;15(2):111–122. DOI: 10.1111/j.1600-0765.1980.tb00265.x.
  42. Mariotti A. Sex steroid hormones and cell dynamics in the periodontium. Crit Rev Oral Biol Med 1994;5(1):27–53. DOI: 10.1177/10454411940050010201.
  43. Deasy MJ, Vogel RI. Female sex hormonal factors in periodontal disease. Ann Dent 1976;35(3):42–46. PMID: 788632.
  44. Mealey BL, Moritz AJ. Hormonal influences: effects of diabetes mellitus and endogenous female sex steroid hormones on the periodontium. Periodontol 2000 2003;32:59–81. DOI: 10.1046/j.0906-6713.2002.03206.x.
  45. Vittek J, Hernandez MR, Wenk EJ, et al. Specific estrogen receptors in human gingiva. J Clin Endocrinol Metab 1982;54(3):608–612. DOI: 10.1210/jcem-54-3-608.
  46. Lewko WM, Anderson A. Estrogen receptors and growth response in cultured human periodontal ligament cells. Life Sci 1986;39(13): 1201–1206. DOI: 10.1016/0024-3205(86)90352-8.
  47. Kornman KS, Loesche WJ. Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis. Infect Immun 1982;35(1):256–263. DOI: 10.1128/iai.35.1.256-263.1982.
  48. Carrillo-De-Albornoz A, Figuero E, Herrera D, et al. Gingival changes during pregnancy: II. Influence of hormonal variations on the subgingival biofilm. J Clin Periodontol 2010;37(3):230–240. DOI: 10.1111/j.1600-051X.2009.01514.x.
  49. Yokoyama M, Hinode D, Yoshioka M, et al. Relationship between Campylobacter rectus and periodontal status during pregnancy. Oral Microbiol Immunol 2008;23(1):55–59. DOI: 10.1111/j.1399-302X.2007.00391.x.
  50. Piccinni MP. T cell tolerance towards the fetal allograft. J Reprod Immunol 2010;85(1):71–75. DOI: 10.1016/j.jri.2010.01.006.
  51. Björksten B, Söderström T, Damber MG, et al. Polymorphonuclear leucocyte function during pregnancy. Scand J Immunol 1978;8(3): 257–262. DOI: 10.1111/j.1365-3083.1978.tb00518.x.
  52. Persellin RH, Thoi LL. Human polymorphonuclear leukocyte phagocytosis in pregnancy. Development of inhibition during gestation and recovery in the postpartum period. Am J Obstet Gynecol 1979;134(3):250–255. DOI: 10.1016/S0002-9378(16)33028-9.
  53. El-Maallem H, Fletcher J. Impaired neutrophil function and myeloperoxidase deficiency in pregnancy. Br J Haematol 1980;44(3):375–381. DOI: 10.1111/j.1365-2141.1980.tb05906.x.
  54. Krause PJ, Ingardia CJ, Pontius LT, et al. Host defense during pregnancy: neutrophil chemotaxis and adherence. Am J Obstet Gynecol 1987;157(2):274–280. DOI: 10.1016/S0002-9378(87)80150-3.
  55. Yokoyama M, Hinode D, Masuda K, et al. Effect of female sex hormones on Campylobacter rectus and human gingival fibroblasts. Oral Microbiol Immunol 2005;20(4):239–243. DOI: 10.1111/j.1399-302X.2005.00222.x.
  56. Shu L, Guan SM, Fu SM, et al. Estrogen modulates cytokine expression in human periodontal ligament cells. J Dent Res 2008;87(2):142–147. DOI: 10.1177/154405910808700214.
  57. Smith JM, Shen Z, Wira CR, et al. Effects of menstrual cycle status and gender on human neutrophil phenotype. Am J Reprod Immunol 2007;58(2):111–119. DOI: 10.1111/j.1600-0897.2007.00494.x.
  58. Miyagi M, Morishita M, Iwamoto Y. Effects of sex hormones on production of prostaglandin E 2 by human peripheral monocytes. J Periodontol 1993;64(11):1075–1078. DOI: 10.1902/jop.1993.64.11.1075.
  59. Morishita M, Miyagi M, Iwamoto Y. Effects of sex hormones on production of interleukin-1 by human peripheral monocytes. J Periodontol 1999;70(7):757–760. DOI: 10.1902/jop.1999.70.7.757.
  60. Bieri RA, Adriaens L, Spörri S, et al. Gingival fluid cytokine expression and subgingival bacterial counts during pregnancy and postpartum: a case series. Clin Oral Investig 2013;17(1):19–28. DOI: 10.1007/s00784-012-0674-8.
  61. Haerian-Ardakani A, Moeintaghavi A, Talebi-Ardakani MR, et al. The association between current low-dose oral contraceptive pills and periodontal health: a matched-case-control study. J Contemp Dent Pract 2010;11(3):33–40. DOI: 10.5005/jcdp-11-3-33.
  62. Khalighinejad N, Aminoshariae A, Kulild JC, et al. Apical periodontitis, a predictor variable for preeclampsia: a case-control study. J Endod 2017;43(10):1611–1614. DOI: 10.1016/j.joen.2017.05.021.
  63. Kumar A, Sharma DS, Verma M, et al. Association between periodontal disease and gestational diabetes mellitus—a prospective cohort study. J Clin Periodontol 2018;45(8):920–931. DOI: 10.1111/jcpe.12902.
  64. Figueiredo MGOP, Takita SY, Dourado BMR, et al. Periodontal disease: repercussions in pregnant woman and newborn health—a cohort study. PLoS One 2019;14(11):e0225036. DOI: 10.1371/journal.pone.0225036.
  65. Mathew RJ, Bose A, Prasad JH, et al. Maternal periodontal disease as a significant risk factor for low birth weight in pregnant women attending a secondary care hospital in South India: a case-control study. Indian J Dent Res 2014;25(6):742–747. DOI: 10.4103/0970-9290.152184.
  66. Bi WG, Emami E, Luo ZC, et al. Effect of periodontal treatment in pregnancy on perinatal outcomes: a systematic review and meta-analysis. J Matern Neonatal Med 2019;34(19):3259–3268. DOI: 10.1080/14767058.2019.1678142.
  67. Offenbacher S, Katz V, Fertik G, et al. Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 1996;67(Suppl 10):1103–1113. DOI: 10.1902/jop.1996.67.10s.1103.
  68. Jeffcoat MK, Geurs NC, Reddy MS, et al. Periodontal infection and preterm birth: results of a prospective study. J Am Dent Assoc 2001;132(7):875–880. DOI: 10.14219/jada.archive.2001.0299.
  69. Offenbacher S, Lieff S, Boggess KA, et al. Maternal periodontitis and prematurity. Part I: obstetric outcome of prematurity and growth restriction. Ann Periodontol 2001;6(1):164–174. DOI: 10.1902/annals.2001.6.1.164.
  70. Davenport ES, Williams CECS, Sterne JAC, et al. Maternal periodontal disease and preterm low birthweight: case-control study. J Dent Res 2002;81(5):313–318. DOI: 10.1177/154405910208100505.
  71. Corbella S, Taschieri S, Del Fabbro M, et al. Adverse pregnancy outcomes and periodontitis: a systematic review and meta-analysis exploring potential association. Quintessence Int (Berl) 2016;47(3):193–204. DOI: 10.3290/j.qi.a34980.
  72. Ide M, Papapanou PN. Epidemiology of association between maternal periodontal disease and adverse pregnancy outcomes – systematic review. J Clin Periodontol 2013;40 Suppl 14:S181–S94. DOI: 10.1111/jcpe.12063.
  73. Baskaradoss JK, Geevarghese A, Al Dosari AAF. Causes of adverse pregnancy outcomes and the role of maternal periodontal status – a review of the literature. Open Dent J 2012;6:79–84. DOI: 10.2174/1874210601206010079.
  74. Corbella S, Taschieri S, Francetti L, et al. Periodontal disease as a risk factor for adverse pregnancy outcomes: a systematic review and meta-analysis of case-control studies. Odontology 2012;100(2):232–240. DOI: 10.1007/s10266-011-0036-z.
  75. Konopka T, Paradowska-Stolarz A. Periodontitis and risk of preterm birth and low birthweight–a meta-analysis. Ginekol Pol 2012;83(6):446–453. PMID: 22880465.
  76. Shanthi V, Vanka A, Bhambal A, et al. Association of pregnant women periodontal status to preterm and low-birth weight babies: a systematic and evidence-based review. Dent Res J (Isfahan) 2012;9(4):368–380. PMID: 23162575.
  77. Offenbacher S, Beck JD, Jared HL, et al. Effects of periodontal therapy on rate of preterm delivery: a randomized controlled trial. Obstet Gynecol 2009;114(3):551–559. DOI: 10.1097/AOG. 0b013e3181b1341f.
  78. Michalowicz BS, Hodges JS, DiAngelis AJ, et al. Treatment of periodontal disease and the risk of preterm birth. N Engl J Med 2006;355(18):1885–1894. DOI: 10.1056/NEJMoa062249.
  79. López NJ, Smith PC, Gutierrez J. Periodontal therapy may reduce the risk of preterm low birth weight in women with peridotal disease: a randomized controlled trial. J Periodontol 2002;73(8):911–924. DOI: 10.1902/jop.2002.73.8.911.
  80. Romero R, Espinoza J, Kusanovic JP, et al. The preterm parturition syndrome. BJOG An Int J Obstet Gynaecol 2006;113 (Suppl 3): 17–42. DOI: 10.1111/j.1471-0528.2006.01120.x.
  81. Gilles HM, Lawson JB, Sibelas M, et al. Malaria, anaemia and pregnancy. Ann Trop Med Parasitol 1969;63(2):245–263. DOI: 10.1080/00034983.1969.11686625.
  82. Osman NB, Folgosa E, Gonzales C, et al. Genital infections in the aetiology of late fetal death: an incident case-referent study. J Trop Pediatr 1995;41(5):258–266. DOI: 10.1093/tropej/41.5.258.
  83. Benedetti TJ, Valle R, Ledger WJ. Antepartum pneumonia in pregnancy. Am J Obstet Gynecol 1982;144(4):413–417. DOI: 10.1016/0002-9378(82)90246-0.
  84. Madinger NE, Greenspoon JS, Ellrodt AG. Pneumonia during pregnancy: has modern technology improved maternal and fetal outcome? Am J Obstet Gynecol 1989;161(3):657–662. DOI: 10.1016/0002-9378(89)90373-6.
  85. Hibbard L, Thrupp L, Summeril S, et al. Treatment of pyelonephritis in pregnancy. Am J Obstet Gynecol 1967;98(5):609–615. DOI: 10.1016/0002-9378(67)90172-X.
  86. Cunningham FG, Morris GB, Mickal A. Acute pyelonephritis of pregnancy: a clinical review. Obstet Gynecol 1973;42(1):112–117. PMID: 4720190.
  87. Herd N, Jordan T. An investigation of malaria during pregnancy in Zimbabwe. Cent Afr J Med 1981;27:62–68. PMID: 7261055.
  88. Kalanda BF, Verhoeff FH, Chimsuku L, et al. Adverse birth outcomes in a malarious area. Epidemiol Infect 2006;134(3):659–666. DOI: 10.1017/S0950268805005285.
  89. Patrick MJ. Influence of maternal renal infection on the foetus and infant. Arch Dis Child 1967;42(222):208–213. DOI: 10.1136/adc.42.222.208.
  90. Wren BG. Subclinical renal infection and prematurity. Med J Aust 1969;2(12):596–600. DOI: 10.5694/j.1326-5377.1969.tb107290.x.
  91. Munn MB, Groome LJ, Atterbury JL, et al. Pneumonia as a complication of pregnancy. J Matern Neonatal Med 1999;8(4):151. DOI: 10.1002/(sici)1520-6661(199907/08)8:4<151::aid-mfm2>3.0.co;2-h.
  92. Kaul AK, Khan S, Martens MG, et al. Experimental gestational pyelonephritis induces preterm births and low birth weights in C3H/HeJ mice. Infect Immun 1999;67(11):5958–5966. DOI: 10.1128/iai.67.11.5958-5966.1999.
  93. Romero R, Mazor M, Munoz H, et al. The preterm labor syndrome. Ann N Y Acad Sci 1994;734:414–429. DOI: 10.1111/j.1749-6632.1994.tb21771.x.
  94. Minkoff H. Prematurity: infection as an etiologic factor. Obstet Gynecol 1983;62(2):137–144. PMID: 6346172.
  95. Romero R, Mazor M, Ying King Wu, et al. Infection in the pathogenesis of preterm labor. Semin Perinatol 1988;12(4):262–279. DOI: 10.5555/uri:pii:0146000588900456.
  96. Romero R, Sirtori M, Oyarzun E, et al. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am J Obstet Gynecol 1989;161(3):817–824. DOI: 10.1016/0002-9378(89)90409-2.
  97. Gonçalves LF, Chaiworapongsa T, Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev 2002;8(1):3–13. DOI: 10.1002/mrdd.10008.
  98. Zahl PA, Bjerknes C. Induction of decidua-placental hemorrhage in mice by the endotoxins of certain gram-negative bacteria. Proc Soc Exp Biol Med 1943;54(3):329. DOI: 10.3181/00379727-54-14424.
  99. Elovitz MA, Mrinalini C. Animal models of preterm birth. Trends Endocrinol Metab 2004;15(10):479–487. DOI: 10.1016/j.tem.2004.10.009.
  100. Fidel PL, Romero R, Wolf N, et al. Systemic and local cytokine profiles in endotoxin-induced preterm parturition in mice. Am J Obstet Gynecol 1994;170(5 Pt 1):1467–1475. DOI: 10.1016/S0002-9378(94)70180-6.
  101. Hirsch E, Saotome I, Hirsch D. A model of intrauterine infection and preterm delivery in mice. Am J Obstet Gynecol 1995;172(5):1598–1603. DOI: 10.1016/0002-9378(95)90503-0.
  102. Gibbs RS, McDuffie RS, Kunze M, et al. Experimental intrauterine infection with Prevotella bivia in New Zealand White rabbits. Am J Obstet Gynecol 2004;190(4):1082–1086. DOI: 10.1016/j.ajog.2003.10.700.
  103. McKay DG, Wong TC. The effect of bacterial endotoxin on the placenta of the rat. Am J Pathol 1963;42(3):357–377. PMID: 19971021.
  104. Kullander S. Fever and parturition an experimental study in rabbits. Acta Obstet Gynecol Scand 1977;66:77–85. DOI: 10.3109/00016347709156356.
  105. McDuffie RS, Sherman MP, Gibbs RS. Amniotic fluid tumor necrosis factor-a and interleukin-1 in a rabbit model of bacterially induced preterm pregnancy loss. Am J Obstet Gynecol 1992;167(6):1583–1588. DOI: 10.1016/0002-9378(92)91745-V.
  106. Gravett MG, Witkin SS, Haluska GJ, et al. An experimental model for intraamniotic infection and preterm labor in rhesus monkeys. Am J Obstet Gynecol 1994;171(6):1660–1667. DOI: 10.1016/0002-9378(94)90418-9.
  107. Wang H, Hirsch E. Bacterially-induced preterm labor and regulation of prostaglandin-metabolizing enzyme expression in mice: the role of toll-like receptor 41. Biol Reprod 2003;69(6):1957–1963. DOI: 10.1095/biolreprod.103.019620.
  108. Fidel P, Ghezzi F, Romero R, et al. The effect of antibiotic therapy on intrauterine infection-induced preterm parturition in rabbits. J Matern Neonatal Med 2003;14(1):57–64. DOI: 10.1080/jmf.14.1.57.64.
  109. Romero R, Oyarzun E, Mazor M, et al. Meta-analysis of the relationship between asymptomatic bacteriuria and preterm delivery/low birth weight. Obstet Gynecol 1989;73(4):576–582. PMID: 2927852.
  110. Smaill FM, Vazquez JC. Antibiotics for asymptomatic bacteriuria in pregnancy. Cochrane Database Syst Rev 2019;2019(11):CD000490. DOI: 10.1002/14651858.CD000490.pub4.
  111. Fazeli A, Bruce C, Anumba DO. Characterization of Toll-like receptors in the female reproductive tract in humans. Hum Reprod 2005;20(5):1372–1378. DOI: 10.1093/humrep/deh775.
  112. Elovitz MA, Wang Z, Chien EK, et al. A new model for inflammation-induced preterm birth: the role of platelet-activating factor and toll-like receptor-4. Am J Pathol 2003;163(5):2103–2111. DOI: 10.1016/S0002-9440(10)63567-5.
  113. Abrahams VM, Bole-Aldo P, Kim YM, et al. Divergent trophoblast responses to bacterial products mediated by TLRs. J Immunol 2004;173(7):4286–4296. DOI: 10.4049/jimmunol.173.7.4286.
  114. Vadillo Ortega F, Avila Vergara MA, Hernández Guerrero C, et al. [Apoptosis in trophoblast of patients with recurrent spontaneous abortion of unidentified cause]. Ginecol Obstet Mex 2000;68:122–131. PMID: 10808617.
  115. Murthi P, Kee MW, Gude NM, et al. Fetal growth restriction is associated with increased apoptosis in the chorionic trophoblast cells of human fetal membranes. Placenta 2005;26(4):329–338. DOI: 10.1016/j.placenta.2004.07.006.
  116. Huppertz B, Hemmings D, Renaud SJ, et al. Extravillous trophoblast apoptosis – a workshop report. Placenta 2005;26:S46. DOI: 10.1016/j.placenta.2005.02.002.
  117. Romero R, Mazor M, Tartakovsky B. Systemic administration of interleukin-1 induces preterm parturition in mice. Am J Obstet Gynecol 1991;165(4 Pt 1):969–971. DOI: 10.1016/0002-9378(91) 90450-6.
  118. Watari M, Watari H, DiSanto ME, et al. Pro-inflammatory cytokines induce expression of matrix-metabolizing enzymes in human cervical smooth muscle cells. Am J Pathol 1999;154(6):1755–1762. DOI: 10.1016/S0002-9440(10)65431-4.
  119. Fortunato SJ, Menon R, Lombardi SJ. Role of tumor necrosis factor-α in the premature rupture of membranes and preterm labor pathways. Am J Obstet Gynecol 2002;187(5):1159–1162. DOI: 10.1067/mob.2002.127457.
  120. Athayde N, Edwin SS, Romero R, et al. A role for matrix metalloproteinase-9 in spontaneous rupture of the fetal membranes. Am J Obstet Gynecol 1998;179(5):1248–1253. DOI: 10.1016/S0002-9378(98)70141-3.
  121. Maymon E, Romero R, Pacora P, et al. Evidence of in vivo differential bioavailability of the active forms of matrix metalloproteinases 9 and 2 in parturition, spontaneous rupture of membranes, and intra-amniotic infection. Am J Obstet Gynecol 2000;183(4):887–894. DOI: 10.1067/mob.2000.108878.
  122. Romero R, Chaiworapongsa T, Espinoza J, et al. Fetal plasma MMP-9 concentrations are elevated in preterm premature rupture of the membranes. Am J Obstet Gynecol 2002;187(5):1125–1130. DOI: 10.1067/mob.2002.127312.
  123. Osmers RGW, Adelmann-Grill BC, Rath W, et al. Biochemical events in cervical ripening dilatation during pregnancy and parturition. J Obstet Gynaecol (Lahore) 1995;21(2):185–194. DOI: 10.1111/j.1447-0756.1995.tb01092.x.
  124. Rath W, Winkler M, Kemp B. The importance of extracellular matrix in the induction of preterm delivery. J Perinat Med 1998;26(6):437. DOI: 10.1515/jpme.1998.26.6.437.
  125. Hirsch E, Muhle RA, Mussalli GM, et al. Bacterially induced preterm labor in the mouse does not require maternal interleukin-1 signaling. Am J Obstet Gynecol 2002;186(3):523–530. DOI: 10.1067/mob.2002.120278.
  126. Hirsch E, Filipovich Y, Mahendroo M. Signaling via the type I IL-1 and TNF receptors is necessary for bacterially induced preterm labor in a murine model. Am J Obstet Gynecol 2006;194(5):1334–1340. DOI: 10.1016/j.ajog.2005.11.004.
  127. Romero R, Tartakovsky B. The natural interleukin-1 receptor antagonist prevents interleukin-l-induced preterm delivery in mice. Am J Obstet Gynecol 1992;167(4 Pt 1):1041–1045. DOI: 10.1016/S0002-9378(12)80035-4.
  128. 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(2):606–612. DOI: 10.1016/0002-9378(95)90290-2.
  129. Romero R, Avila C, Santhanam U, et al. Amniotic fluid interleukin 6 in preterm labor: association with infection. J Clin Invest 1990;85(5):1392–1400. DOI: 10.1172/JCI114583.
  130. Cox SM. Interleukin-1 beta, -1 alpha, and -6 and prostaglandins in vaginal/cervical fluids of pregnant women before and during labor. J Clin Endocrinol Metab 1993. DOI: 10.1210/jc.77.3.805.
  131. Hillier SL, Witkin SS, Krohn MA, et al. The relationship of amniotic fluid cytokines and preterm delivery, amniotic fluid infection, histologic chorioamnionitis, and chorioamnion infection. Obstet Gynecol 1993;81(6):941–948. PMID: 8497360.
  132. Gomez R, Romero R, Galasso M, et al. The value of amniotic fluid interleukin-6, white blood cell count, and gram stain in the diagnosis of microbial invasion of the amniotic cavity in patients at term. Am J Reprod Immunol 1994;32(3):200–210. DOI: 10.1111/j.1600-0897.1994.tb01115.x.
  133. Messer J, Eyer D, Donato L, et al. Evaluation of interleukin-6 and soluble receptors of tumor necrosis factor for early diagnosis of neonatal infection. J Pediatr 1996;129(4):574–580. DOI: 10.1016/S0022-3476(96)70123-3.
  134. Athayde N, Romero R, Maymon E, et al. Interleukin 16 in pregnancy, parturition, rupture of fetal membranes, and microbial invasion of the amniotic cavity. Am J Obstet Gynecol 2000;182(1 Pt 1):135–141. DOI: 10.1016/S0002-9378(00)70502-3.
  135. Pacora P, Romero R, Maymon E, et al. Participation of the novel cytokine interleukin 18 in the host response to intra-amniotic infection. Am J Obstet Gynecol 2000;183(5):1138–1143. DOI: 10.1067/mob.2000.108881.
  136. Hanna N, Hanna I, Hleb M, et al. Gestational age-dependent expression of IL-10 and its receptor in human placental tissues and isolated cytotrophoblasts. J Immunol 2000;164(11):5721–5728. DOI: 10.4049/jimmunol.164.11.5721.
  137. Sadowsky DW, Novy MJ, Witkin SS, et al. Dexamethasone or interleukin-10 blocks interleukin-1beta-induced uterine contractions in pregnant rhesus monkeys. Am J Obstet Gynecol 2003;188(1):252–263. DOI: 10.1067/mob.2003.70.
  138. Terrone DA, Rinehart BK, Granger JP, et al. Interleukin-10 administration and bacterial endotoxin-induced preterm birth in a rat model. Obstet Gynecol 2001;98(3):476–480. DOI: 10.1016/S0029-7844(01)01424-7.
  139. Rodts-Palenik S, Wyatt-Ashmead J, Pang Y, et al. Maternal infection-induced white matter injury is reduced by treatment with interleukin-10. Am J Obstet Gynecol 2004;191(4):1387–1392. DOI: 10.1016/j.ajog.2004.06.093.
  140. Aagaard K, Ma J, Antony KM, et al. The placenta harbors a unique microbiome. Sci Transl Med 2014;6(237):237ra65. DOI: 10.1126/scitranslmed.3008599.
  141. Bearfield C, Davenport ES, Sivapathasundaram V, et al. Possible association between amniotic fluid micro-organism infection and microflora in the mouth. British journal of obstetrics and gynaecology 2002;109(5):527–533. DOI: 10.1111/j.1471-0528.2002.01349.x.
  142. Han YW, Ikegami A, Bissada NF, et al. Transmission of an uncultivated Bergeyella strain from the oral cavity to amniotic fluid in a case of preterm birth. J Clin Microbiol 2006;44(4):1475–1483. DOI: 10.1128/JCM.44.4.1475-1483.2006.
  143. Muwazi L, Rwenyonyi CM, Nkamba M, et al. Periodontal conditions, low birth weight and preterm birth among postpartum mothers in two tertiary health facilities in Uganda. BMC Oral Health 2014;14:42. DOI: 10.1186/1472-6831-14-42.
  144. Sánchez AR, Bagniewski S, Weaver AL, et al. Correlations between maternal periodontal conditions and preterm low birth weight infants. J Int Acad Periodontol 2007;9(2):34–41. PMID: 17506382.
  145. Yeo BK, Lim LP, Paquette DW, et al. Periodontal disease–the emergence of a risk for systemic conditions: pre-term low birth weight. Ann Acad Med Singapore 2005;34(1):111–116. PMID: 15726229.
  146. Johnson S, Evans TA, Draper ES, et al. Neurodevelopmental outcomes following late and moderate prematurity: a population-based cohort study. Arch Dis Child Fetal Neonatal Ed 2015;100(4):F301–F308. DOI: 10.1136/archdischild-2014-307684.
  147. Poulsen G, Wolke D, Kurinczuk JJ, et al. Gestational age and cognitive ability in early childhood: a population-based cohort study. Paediatr Perinat Epidemiol 2013;27(4):371–379. DOI: 10.1111/ppe.12058.
  148. Kerstjens JM, De Winter AF, Bocca-Tjeertes IF, et al. Developmental delay in moderately preterm-born children at school entry. J Pediatr 2011;159(1):92–98. DOI: 10.1016/j.jpeds.2010.12.041.
  149. Boyle EM, Poulsen G, Field DJ, et al. Effects of gestational age at birth on health outcomes at 3 and 5 years of age: population based cohort study. British Medical Association 2012;344:e896. DOI: 10.1136/bmj.e896.
  150. Cserjési R, Van Braeckel KNJA, Butcher PR, et al. Functioning of 7-year-old children born at 32–35 weeks’ gestational age. Pediatrics 2012;130(4):e838–e846. DOI: 10.1542/peds.2011-2079.
  151. Talge NM, Holzman C, Wang J, et al. Late-preterm birth and its association with cognitive and socioemotional outcomes at 6 years of age. Pediatrics 2010;126(6):1124–1131. DOI: 10.1542/peds. 2010-1536.
  152. Mackay DF, Smith GCS, Dobbie R, et al. Gestational age at delivery and special educational need: retrospective cohort study of 407,503 schoolchildren. PLoS Med 2010;7(6):e1000289. DOI: 10.1371/journal.pmed.1000289.
  153. Lipkind HS, Slopen ME, Pfeiffer MR, et al. School-age outcomes of late preterm infants in New York City. Am J Obstet Gynecol 2012;206(3):222.e1–e6. DOI: 10.1016/j.ajog.2012.01.007.
  154. Quigley MA, Poulsen G, Boyle E, et al. Early term and late preterm birth are associated with poorer school performance at age 5 years: a cohort study. Arch Dis Child Fetal Neonatal Ed 2012;97(3):F167–F173. DOI: 10.1136/archdischild-2011-300888.
  155. Mathiasen R, Hansen BM, Nybo Andersen AMN, et al. Gestational age and basic school achievements: a national follow-up study in Denmark. Pediatrics 2010;126(6):e1553–e1561. DOI: 10.1542/peds.2009-0829.
  156. Chyi LJ, Lee HC, Hintz SR, et al. School outcomes of late preterm infants: special needs and challenges for infants born at 32–36 weeks gestation. J Pediatr 2008;153(1):25–31. DOI: 10.1016/j.jpeds.2008.01.027.
  157. Potijk MR, De Winter AF, Bos AF, et al. Higher rates of behavioural and emotional problems at preschool age in children born moderately preterm. Arch Dis Child 2012;97(2):112–117. DOI: 10.1136/adc.2011.300131.
  158. Favrais G, Van De Looij Y, Fleiss B, et al. Systemic inflammation disrupts the developmental program of white matter. Ann Neurol 2011;70(4):550–565. DOI: 10.1002/ana.22489.
  159. Smith PLP, Hagberg H, Naylor AS, et al. Neonatal peripheral immune challenge activates microglia and inhibits neurogenesis in the developing murine hippocampus. Dev Neurosci 2014;36(2):119–131. DOI: 10.1159/000359950.
  160. Boksa P. Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav Immun 2010;24(6):881–897. DOI: 10.1016/j.bbi.2010.03.005.
  161. Tahraoui SL, Marret S, Bodénant C, et al. Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol 2001;11(1):56–71. DOI: 10.1111/j.1750-3639.2001.tb00381.x.
  162. Rousset CI, Chalon S, Cantagrel S, et al. Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr Res 2006;59(3):428–433. DOI: 10.1203/01.pdr.0000199905.08848.55.
  163. Covey MV, Loporchio D, Buono KD, et al. Opposite effect of inflammation on subventricular zone versus hippocampal precursors in brain injury. Ann Neurol 2011;70(4):616–626. DOI: 10.1002/ana.22473.
  164. Lively S, Schlichter LC. Microglia responses to pro-inflammatory stimuli (LPS, IFNγ+TNFα) and reprogramming by resolving cytokines (IL-4, IL-10). Front Cell Neurosci 2018;12:215. DOI: 10.3389/fncel.2018.00215.
  165. Golan H, Levav T, Mendelsohn A, et al. Involvement of tumor necrosis factor alpha in hippocampal development and function. Cereb Cortex 2004;14(1):97–105. DOI: 10.1093/cercor/bhg108.
  166. Aloe L, Properzi F, Probert L, et al. Learning abilities, NGF and BDNF brain levels in two
PDF Share
PDF Share

© Jaypee Brothers Medical Publishers (P) LTD.