Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-24T05:47:38.727Z Has data issue: false hasContentIssue false
  • English
  • Français

Causal role of group B Streptococcus-induced acute chorioamnionitis in intrauterine growth retardation and cerebral palsy-like impairments

Published online by Cambridge University Press:  10 January 2019

M.-J. Allard ,
M.-E. Brochu ,
J. D. Bergeron ,
M. Segura  and
G. Sébire
M.-J. Allard
Affiliation:
Department of Pediatrics, McGill University, Montreal, QC, Canada
M.-E. Brochu
Affiliation:
Department of Pediatrics, Université de Sherbrooke, Sherbrooke, QC, Canada
J. D. Bergeron
Affiliation:
Department of Pediatrics, Université de Sherbrooke, Sherbrooke, QC, Canada
M. Segura
Affiliation:
Department of Infectiology and Microbiology, Université de Montréal, Saint-Hyacinthe, QC, Canada
G. Sébire*
Affiliation:
Department of Pediatrics, McGill University, Montreal, QC, Canada Department of Pediatrics, Université de Sherbrooke, Sherbrooke, QC, Canada
*
Address for correspondence: Dr G. Sébire, Research Institute of the McGill University Health Centre – Glen site, 1001, Decarie Boulevard, Montreal, QC, Canada H4A 3J1. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Chorioamnionitis and intrauterine growth retardation (IUGR) are risk factors for cerebral palsy (CP). Common bacteria isolated in chorioamnionitis include group B Streptococcus (GBS) serotypes Ia and III. Little is known about the impact of placental inflammation induced by different bacteria, including different GBS strains. We aimed to test the impact of chorioamnionitis induced by two common GBS serotypes (GBSIa and GBSIII) on growth and neuromotor outcomes in the progeny. Dams were exposed at the end of gestation to either saline, inactivated GBSIa or GBSIII. Inactivated GBS bacteria invaded placentas and triggered a chorioamnionitis featured by massive polymorphonuclear cell infiltrations. Offspring exposed to GBSIII – but not to GBSIa – developed IUGR, persisting beyond adolescent age. Male rats in utero exposed to GBSIII traveled a lower distance in the Open Field test, which was correlating with their level of IUGR. GBSIII-exposed rats presented decreased startle responses to acoustic stimuli beyond adolescent age. GBS-exposed rats displayed a dysmyelinated white matter in the corpus callosum adjacent to thinner primary motor cortices. A decreased density of microglial cells was detected in the mature corpus callosum of GBSIII-exposed males – but not females – which was correlating positively with the primary motor cortex thickness. Altogether, our results demonstrate a causal link between pathogen-induced acute chorioamnionitis and (1) IUGR, (2) serotype- and sex-specific neuromotor impairments and (3) abnormal development of primary motor cortices, dysmyelinated white matter and decreased density of microglial cells.

Keywords

chorioamnionitisIUGRmotor cortexrat, white matter injuries
Type
Brief Report
Information
Journal of Developmental Origins of Health and Disease , Volume 10 , Issue 5 , October 2019 , pp. 595 - 602
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Tita, ATN, Andrews, WW. Diagnosis and management of clinical chorioamnionitis. Clin Perinatol. 2010; 37, 339–354.CrossRefGoogle ScholarPubMed
Sperling, RS, Newton, E, Gibbs, RS. Intraamniotic infection in low-birth-weight infants. J Infect Dis. 1988; 157, 113–117.CrossRefGoogle ScholarPubMed
Pugni, L, Pietrasanta, C, Acaia, B, et al. Chorioamnionitis and neonatal outcome in preterm infants: a clinical overview. J Matern Fetal Neonatal Med. 2016; 29, 1525–1529.CrossRefGoogle ScholarPubMed
Galinsky, R, Polglase, GR, Hooper, SB, Black, MJ, Moss, TJM. The consequences of chorioamnionitis: preterm birth and effects on development. J Pregnancy. 2013; 2013, 412831.CrossRefGoogle ScholarPubMed
Ruff, CA, Faulkner, SD, Rumajogee, P, et al. The extent of intrauterine growth restriction determines the severity of cerebral injury and neurobehavioural deficits in rodents. PLoS One. 2017; 12, e0184653.CrossRefGoogle ScholarPubMed
Tolcos, M, Petratos, S, Hirst, JJ, et al. Blocked, delayed, or obstructed: What causes poor white matter development in intrauterine growth restricted infants? Prog Neurobiol. 2017; 154, 62–77.CrossRefGoogle ScholarPubMed
Spencer, SJ, Meyer, U. Perinatal programming by inflammation. Brain Behav Immun. 2017; 63, 1–7.CrossRefGoogle ScholarPubMed
Schendel, DE, Schuchat, A, Thorsen, P. Public health issues related to infection in pregnancy and cerebral palsy. Ment Retard Dev Disabil Res Rev. 2002; 8, 39–45.CrossRefGoogle ScholarPubMed
Romero, R, Gomez, R, Ghezzi, F, et al. A fetal systemic inflammatory response is followed by the spontaneous onset of preterm parturition. Am J Obstet Gynecol. 1998; 179, 186–193.CrossRefGoogle ScholarPubMed
Zhang, Q, Lu, HY, Wang, JX, et al. Relationship between placental inflammation and fetal inflammatory response syndrome and brain injury in preterm infants. Zhongguo Dang Dai Er Ke Za Zhi. 2015; 17, 217–221.Google ScholarPubMed
Gotsch, F, Romero, R, Kusanovic, JP, et al. The fetal inflammatory response syndrome. Clin Obstet Gynecol. 2007; 50, 652–683.CrossRefGoogle ScholarPubMed
Patras, KA, Nizet, V. Group B Streptococcal Maternal Colonization and Neonatal Disease: Molecular Mechanisms and Preventative Approaches. Front Pediatr. 2018; 6, 27.CrossRefGoogle Scholar
Regan, JA, Klebanoff, MA, Nugent, RP, et al. Colonization with group B streptococci in pregnancy and adverse outcome. Am J Obstet Gynecol. 1996; 174, 1354–1360.CrossRefGoogle Scholar
Teatero, S, Ferrieri, P, Martin, I, et al. Serotype distribution, population structure, and antimicrobial resistance of group b streptococcus strains recovered from colonized pregnant women. J Clin Microbiol. 2017; 55, 412–422.CrossRefGoogle ScholarPubMed
Lu, B, Wu, J, Chen, X, et al. Microbiological and clinical characteristics of Group B Streptococcus isolates causing materno-neonatal infections: high prevalence of CC17/PI-1 and PI-2b sublineage in neonatal infections. J Med Microbiol. 2018; 67, 1551–1559.CrossRefGoogle ScholarPubMed
O’Riordan, K, Lee, JC. Staphylococcus aureus capsular polysaccharides. Clin Microbiol Rev. 2004; 17, 218–234.CrossRefGoogle ScholarPubMed
Lemire, P, Houde, M, Lecours, MP, Fittipaldi, N, Segura, M. Role of capsular polysaccharide in Group B Streptococccus interactions with dendritic cells. Microbes Infect. 2012; 14, 1064–1076.CrossRefGoogle Scholar
Joubrel, C, Tazi, A, Six, A, et al. Group B streptococcus neonatal invasive infections, France 2007-2012. Clin Microbiol Infect. 2015; 21, 910–916.CrossRefGoogle ScholarPubMed
Périchon, B, Szili, N, du Merle, L, et al. Regulation of PI-2b pilus expression in hypervirulent Streptococcus agalactiae ST-17 BM110. PLoS One. 2017; 12, e0169840.CrossRefGoogle ScholarPubMed
Andrade, EB, Magalhães, A, Puga, A, et al. A mouse model reproducing the pathophysiology of neonatal group B streptococcal infection. Nat Commun. 2018; 9, 3138.CrossRefGoogle ScholarPubMed
Allard, M-J, Bergeron, JD, Baharnoori, M, et al. A sexually dichotomous, autistic-like phenotype is induced by Group B Streptococcus maternofetal immune activation. Autism Res. 2017; 10, 233–245.CrossRefGoogle ScholarPubMed
Bergeron, J, Gerges, N, Guiraut, C, et al. Activation of the IL-1β/CXCL1/MMP-10 axis in chorioamnionitis induced by inactivated Group B Streptococcus. Placenta. 2016; 47, 116–123.CrossRefGoogle ScholarPubMed
Bergeron, JDL, Deslauriers, J, Grignon, S, et al. White matter injury and autistic-like behavior predominantly affecting male rat offspring exposed to group B streptococcal maternal inflammation. Dev Neurosci. 2013; 35, 504–515.CrossRefGoogle Scholar
Lee, JC, Perez, NE, Hopkins, CA, Pier, GB. Purified capsular polysaccharide-induced immunity to Staphylococcus aureus infection. J Infect Dis. 1988; 157, 723–730.CrossRefGoogle ScholarPubMed
Tobias, J, Svennerholm, AM, Carlin, NI, Lebens, M, Holmgren, J. Construction of a non-toxigenic Escherichia coli oral vaccine strain expressing large amounts of CS6 and inducing strong intestinal and serum anti-CS6 antibody responses in mice. Vaccine. 2011; 29, 8863–8869.CrossRefGoogle ScholarPubMed
Simon, P, Dupuis, R, Costentin, J. Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res. 1994; 61, 59–64.CrossRefGoogle ScholarPubMed
Deslauriers, J, Racine, W, Sarret, P, Grignon, S. Preventive effect of α-lipoic acid on prepulse inhibition deficits in a juvenile two-hit model of schizophrenia. Neuroscience. 2014; 272, 261–270.CrossRefGoogle Scholar
Porambo, M, Phillips, AW, Marx, J, et al. Transplanted glial restricted precursor cells improve neurobehavioral and neuropathological outcomes in a mouse model of neonatal white matter injury despite limited cell survival. Glia. 2015; 63, 452–465.CrossRefGoogle Scholar
Paxinos, G, Watson, C, Calabrese, E, Badea, A. MRI/DTI Atlas of the Rat Brain, 2015. Academic Press: Cambridge, MA.Google Scholar
Brochu, M-E, Girard, S, Lavoie, K, Sébire, G. Developmental regulation of the neuroinflammatory responses to LPS and/or hypoxia-ischemia between preterm and term neonates: an experimental study. J Neuroinflammation. 2011; 8, 55.CrossRefGoogle ScholarPubMed
Wixey, JA, Chand, KK, Colditz, PB, Bjorkman, ST. Review: Neuroinflammation in intrauterine growth restriction. Placenta. 2017; 54, 117–154.CrossRefGoogle ScholarPubMed
Blair, EM, Nelson, KB. Fetal growth restriction and risk of cerebral palsy in singletons born after at least 35 weeks’ gestation. Am J Obstet Gynecol. 2015; 212, 520.e1–7.Google Scholar
Dupin, R, Laurent, JP, Stauder, JE, Saliba, E. Auditory attention processing in 5-year-old children born preterm: evidence from event-related potentials. Dev Med Child Neurol. 2000; 42, 476–480.CrossRefGoogle ScholarPubMed
Ferrari, A, Sghedoni, A, Alboresi, S, Pedroni, E, Lombardi, F. New definitions of 6 clinical signs of perceptual disorder in children with cerebral palsy: an observational study through reliability measures. Eur J Phys Rehabil Med. 2014; 50, 709–716.Google ScholarPubMed
Squarzoni, P, Thion, MS, Garel, S. Neuronal and microglial regulators of cortical wiring: usual and novel guideposts. Front Neurosci. 2015; 9, 238.CrossRefGoogle ScholarPubMed
Paolicelli, RC, Ferretti, MT. Function and Dysfunction of Microglia during Brain Development: Consequences for Synapses and Neural Circuits. Front Synaptic Neurosci. 2017; 9, 9.CrossRefGoogle ScholarPubMed
Tolsa, CB, Zimine, S, Warfield, SK, et al. Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction. Pediatr Res. 2004; 56, 132–138.CrossRefGoogle ScholarPubMed
Hagemeyer, N, Hanft, KM, Akriditou, MA, et al. Microglia contribute to normal myelinogenesis and to oligodendrocyte progenitor maintenance during adulthood. Acta Neuropathol. 2017; 134, 441–458.CrossRefGoogle ScholarPubMed
Winram, SB, Jonas, M, Chi, E, Rubens, CE. Characterization of group B streptococcal invasion of human chorion and amnion epithelial cells in vitro. Infect Immun. 1998; 66, 4932–4941.CrossRefGoogle Scholar
Lemire, P, Roy, D, Fittipaldi, N, et al. Implication of TLR- but not of NOD2-signaling pathways in dendritic cell activation by group B Streptococcus serotypes III and V. PLoS One. 2014; 9, e113940.CrossRefGoogle Scholar
Russell, NJ, Seale, AC, O’Driscoll, M, et al. Maternal Colonization With Group B Streptococcus and Serotype Distribution Worldwide: Systematic Review and Meta-analyses. Clin Infect Dis. 2017; 65, S100–S111.CrossRefGoogle ScholarPubMed
Gilman-Sachs, A, Dambaeva, S, Salazar Garcia, MD, et al. Inflammation induced preterm labor and birth. J Reprod Immunol. 2018; 129, 53–58.CrossRefGoogle ScholarPubMed
Kemp, MW. Preterm birth, intrauterine infection, and fetal inflammation. Front Immunol. 2014; 5, 574.CrossRefGoogle ScholarPubMed
Wang, X, Rousset, CI, Hagberg, H, Mallard, C. Lipopolysaccharide-induced inflammation and perinatal brain injury. Semin Fetal Neonatal Med. 2006; 11, 343–353.CrossRefGoogle ScholarPubMed
Boveri, M, Kinsner, A, Berezowski, V, et al. Highly purified lipoteichoic acid from gram-positive bacteria induces in vitro blood-brain barrier disruption through glia activation: role of pro-inflammatory cytokines and nitric oxide. Neuroscience. 2006; 137, 1193–1209.CrossRefGoogle ScholarPubMed
Supplementary material: File

Allard et al. supplementary material

Table S1

Download Allard et al. supplementary material(File)
File 38.8 KB