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Brain Lesions in Intrauterine Growth Restriction Assessed by Ultrasound Imaging: Focus on US Technique and Periventricular Lesions

  • Nelly Padilla
  • Goya Enriquez
  • Edgar Hernandez-Andrade
  • Angela Arranz
  • Ruthy Acosta-Rojas
  • Eduard Gratacos
Chapter

Abstract

Intrauterine growth-restricted infants constitute a vulnerable population, theoretically at increased risk for brain damage and adverse neurological outcomes. This condition may have specific adverse consequences on brain development, leading to structural and functional brain changes. These adjustments are probably a response against an adverse environment and may lead to a specific pattern of hypoxic-ischemic and/or hemorrhagic ultrasound lesions of distinct severity mainly involving the white matter. Although the results of several studies on abnormal cranial ultrasound findings including hypoxic-ischemic/hemorrhagic lesions are conflicting, the major involvement of intrauterine growth-restricted infants is evident. In addition to periventricular leukomalacia (PVL), transient periventricular echodensities should also be included in the diagnosis of white matter damage. This ultrasound finding has long been considered to have no clinical relevance, but recent reports suggest that transient periventricular echodensities should be regarded as part of the spectrum of white matter damage, since these echodensities might be associated with neurodevelopmental difficulties. Recent long-term postnatal studies have demonstrated that intrauterine growth restriction is specifically associated with significant neurodevelopmental deficits that cannot be attributed to prematurity alone. Neuropsychological alterations appear to particularly affect cognitive functions, suggesting an increased prevalence of white matter injury. The early detection of hypoxic-ischemic and/or hemorrhagic lesions as well as their follow-up through serial cranial ultrasound allows early interventional strategies for improved developmental outcome to be established.

Keywords

White Matter Preterm Neonate White Matter Injury White Matter Damage Periventricular Leukomalacia 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

AGA

Appropriate for gestational age

CT

Computed tomography

GA

Gestational age

IUGR

Intrauterine growth restriction

IVH

Intraventricular hemorrhage

MRI

Magnetic resonance imaging

PVL

Periventricular leukomalacia

TPE

Transient periventricular echodensities

US

Ultrasound

WM

White matter

Notes

Acknowledgments

This work was supported by grants from the Cerebra Foundation for the Brain Injured Child (Carmarthen, Wales, UK) PI 040081, The Thrasher Research Fund (Salt Lake City, USA) 02822-0, Marie Curie Host Fellowships for Early Stage Researchers, FETAL-MED-019707-2, and the Spanish Fondo de Investigaciones Sanitarias (FIS 06/0347). EHA is supported by grants from the Programa Juan de la Cierva para el desarrollo de investigación, Spain.

References

  1. Amato M, Konrad D, Hüppi P, Donati F. Impact of prematurity in intrauterine growth retardation on neonatal hemorrhage and ischemic brain damage. Eur Neurol. 1993;33:299–303.PubMedCrossRefGoogle Scholar
  2. Back SA, Riddle A, McClure MM. Maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke 2007;38:724–30.PubMedCrossRefGoogle Scholar
  3. Baschat AA, Gembruch U, Viscardi RM, Gortner L, Harman R. Antenatal prediction of intraventricular hemorrhage in fetal growth restriction: what is the role of Doppler. Ultrasound Obstet Gynecol. 2002;19:334–39.PubMedCrossRefGoogle Scholar
  4. Benavides-Serralde A, Hernandez-Andrade E, Fernández-Delgado J, Plascencia W, Scheier M, Crispi F, Figueras F, Nicolaides KH, Gratacos E. Use of 3-D ultrasound to calculate the volume of intracranial structures in growth-restricted and appropriated for gestational age fetuses. Ultrasound Obstet Gynecol. 2009;33:530–7.PubMedCrossRefGoogle Scholar
  5. Bernstein IM, Horbar JD, Badger GJ, Ohlsson A, Golan A. Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol. 2000;182:198–206.PubMedCrossRefGoogle Scholar
  6. Bos AF, Einspieler C, Prechtl HF. Intrauterine growth retardation, general movements, and neurodevelopmental outcome: a review. Dev Med Child Neurol. 2001;43:61–8.PubMedCrossRefGoogle Scholar
  7. Chen CC, Huang CB, Chung MY, Huang LT, Yang CY. Periventricular echogenicity is related to delayed neurodevelopment of preterm infants. Am J Perinatol. 2004;21:483–9.PubMedCrossRefGoogle Scholar
  8. Dubois J, Bender M, Borradori-Tolsa C, Cachia A, Lazeyras F, Ha-Vinh Leuchter R, Sizonenko SV, Warfield SK, Mangin JF, Hüppi PS. Primary cortical folding in the human newborn: an early marker of later functional development. Brain 2008;131:2028–41.PubMedCrossRefGoogle Scholar
  9. Enriquez G, Correa F, Lucaya J, Piqueras J, Aso C, Ortega A. Potencial pitfalls in cranial ultrasound. Pediatr Radiol. 2003;33:110–7.PubMedGoogle Scholar
  10. Garite TJ, Clark R, Thorp JA. Intrauterine growth restriction increases morbidity and mortality among premature neonates. Am J Obstet Gynecol. 2004;191:481–7.PubMedCrossRefGoogle Scholar
  11. Geva R, Eshel R, Leitner Y, Fattal-Valevski A, Harel S. Verbal short-term memory span in children: long-term modality dependent effects of intrauterine growth restriction. J Child Psychol Psychiatry 2008;49:1321–30.PubMedCrossRefGoogle Scholar
  12. Gilbert WM, Danielsen B. Pregnancy outcomes associated with intrauterine growth restriction. Am J Obstet Gynecol. 2003;188:1596–601.PubMedCrossRefGoogle Scholar
  13. Hernandez-Andrade E, Figueroa-Diesel H, Jansson T, Rangel-Nava H, Gratacos E. Changes in regional fetal cerebral blood flow perfusion in relation to hemodynamic deterioration in severely growth-restricted fetuses. Ultrasound Obstet Gynecol. 2008;32:71–6.PubMedCrossRefGoogle Scholar
  14. Kutschera J, Tomaselli J, Maurer U, Pichler G, Schwantzer G, Urlesberger B. Minor neurological dysfunction, cognitive development and somatic development at the age of 3 to 11 years in very-low-birthweight infants with transient periventricular echodencities. Acta Paediatr. 2006;95:1577–81.PubMedCrossRefGoogle Scholar
  15. Larroque B, Marret S, Ancel PY, Arnaud C, Marpeau L, Supernant K, Pierrat V, Rozé JC, Matis J, Cambonie G, Burguet A, Andre M, Kaminski M, Bréart G, EPIPAGE Study Group. White matter damage and intraventricular hemorrhage in very preterm infants: the EPIPAGE study. J Pediatr. 2003;143:477–83.PubMedCrossRefGoogle Scholar
  16. Leitner Y, Fattal-Valevski A, Geva R, Eshel R, Toledano-Alhadef H, Rotstein M, Bassan H, Radianu B, Bitchonsky O, Jaffa AJ, Harel S. Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study. J Child Neurol. 2007;22:580–7.PubMedCrossRefGoogle Scholar
  17. Lodygensky GA, Seguier ML, Warfield SK, Borradori Tolsa C, Sizonenko S, Lazeyras F, Hüppi PS. Intrauterine growth restriction affects the preterm infant’s hippocampus. Pediatr Res. 2008;63:438–43.PubMedCrossRefGoogle Scholar
  18. Mari G, Abuhamad AZ, Keller M, Verpairojkit B, Ment L, Copel JA. Is the fetal brain-sparing effect a risk factor for the development of intraventricular hemorrhage in the preterm infant? Ultrasound Obstet Gynecol. 1996;8:329–32.PubMedCrossRefGoogle Scholar
  19. Padilla N, Falcon C, Sanz-Cortés M, Figueras F, Bargalló N, Crispi F, Eixarch E, Arranz A, Botet F, Gratacós E. Differential effects of intrauterine growth restriction on brain structure and development in preterm infants: a magnetic resonance imaging study. Brain Res. 2011;1382:98–108.Google Scholar
  20. Padilla NF, Enriquez G, Jansson T, Gratacos E, Hernandez-Andrade E. Quantitative tissue echogenicity of the neonatal brain assessed by ultrasound imaging. Ultrasound Med Biol. 2009;35:1421–6.PubMedCrossRefGoogle Scholar
  21. Padilla-Gomes NF, Enriquez G, Acosta-Rojas R, Perapoch J, Hernandez-Andrade E, Gratacos E. Prevalence of neonatal ultrasound brain lesions in premature infants with and without growth restriction. Acta Paediatr. 2007;96:1582–7.PubMedCrossRefGoogle Scholar
  22. Pearce WJ. Hypoxic regulation of the fetal cerebral circulation. J Appl Physiol. 2006;100:731–8.PubMedCrossRefGoogle Scholar
  23. Pisani F, Leali L, Moretti S, Turco E, Volante E, Bevilacqua G. Transient periventricular echodensities in preterm and neurodevelopmental outcome. J Child Neurol. 2006;21:230–35.PubMedGoogle Scholar
  24. Resch B, Jammernegg A, Perl E, Riccabona M, Maurer U, Müller WD. Correlation of grading and duration of periventricular echodensities with neurodevelopmental outcome in preterm infants. Pediatr Radiol. 2006;36:810–15.PubMedCrossRefGoogle Scholar
  25. Ress S, Harding R, Walker D. An adverse intrauterine environment: implications for injury and altered development of the brain. Int J Dev Neurosci. 2008;26:3–11.CrossRefGoogle Scholar
  26. Simaeys B, Philips W, Lemahieu I, Govaert P. Quantitative analysis of the neonatal brain by ultrasound. Comput Med Imaging Graph. 2000;24:11–8.PubMedCrossRefGoogle Scholar
  27. Tolsa CB, Zimine S, Warfield SK, Freschi M, Sancho Rossignol A, Lazeyras F, Hanquinet S, Pfizenmaier M, Huppi PS, Verhagen EA, Keating P, ter Horst HJ. Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction. Pediatr Res. 2004;52:132–8.CrossRefGoogle Scholar
  28. Verhagen EA, Keating P, ter Horst HJ, Martjin A, Bos AF. Cerebral oxygen saturation and extraction in preterm infants with transient periventricular echodensities. Pediatrics 2009;124:294–301.PubMedCrossRefGoogle Scholar
  29. Volpe JJ. Neurology of the newborn. 4th ed. Philadelphia, PA: WB Saunders; 2001. pp. 428–93.Google Scholar
  30. Volpe JJ. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2009;8:110–24.PubMedCrossRefGoogle Scholar
  31. de Vries L, Eken P, Dubowitz L. The spectrum of leukomalacia using cranial ultrasound. Behav Brain Res. 1992;49:1–6.PubMedCrossRefGoogle Scholar
  32. Zaw W, Gagnon R, Da Silva O. The risks of adverseneonata outcome among preterm small for gestational age infants according to neonatal versus fetal growth standards. Pediatrics 2003;111:1273–7.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Nelly Padilla
    • 1
    • 2
  • Goya Enriquez
    • 3
  • Edgar Hernandez-Andrade
    • 4
  • Angela Arranz
    • 5
    • 6
  • Ruthy Acosta-Rojas
    • 5
    • 6
  • Eduard Gratacos
    • 5
    • 6
  1. 1.Department of Maternal-Fetal Medicine, ICGONHospital Clinic, Universitat de BarcelonaBarcelonaSpain
  2. 2.Institut D’investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)BarcelonaSpain
  3. 3.Department of Pediatric RadiologyHospital Materno-Infantil de la Vall D’HebrónBarcelonaSpain
  4. 4.Department of Obstetrics and GynecologyPerinatology Research Branch/NICHD/NIH/DHHS, Wayne State University School of MedicineDetroitMI
  5. 5.Department of Maternal-Fetal Medicine, ICGONHospital Clinic, Universitat de BarcelonaBarcelonaSpain
  6. 6.Fetal and Perinatal Medicine Research Group, IDIBAPSHospital Clinic, Universitat de BarcelonaBarcelonaSpain

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