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Pathogenesis and Prevention of Intraventricular Hemorrhage in Preterm Infants

  • Pei-Chen Tsao (Department of Pediatrics, School of Medicine, National Yang Ming Chiao Tung University)
  • 투고 : 2022.12.28
  • 심사 : 2023.03.11
  • 발행 : 2023.05.01

초록

Intraventricular hemorrhage (IVH) is a serious concern for preterm infants and can predispose such infants to brain injury and poor neurodevelopmental outcomes. IVH is particularly common in preterm infants. Although advances in obstetric management and neonatal care have led to a lower mortality rate for preterm infants with IVH, the IVH-related morbidity rate in this population remains high. Therefore, the present review investigated the pathophysiology of IVH and the evidence related to interventions for prevention. The analysis of the pathophysiology of IVH was conducted with a focus on the factors associated with cerebral hemodynamics, vulnerabilities in the structure of cerebral vessels, and host or genetic predisposing factors. The findings presented in the literature indicate that fluctuations in cerebral blood flow, the presence of hemodynamic significant patent ductus arteriosus, arterial carbon dioxide tension, and impaired cerebral venous drainage; a vulnerable or fragile capillary network; and a genetic variant associated with a mechanism underlying IVH development may lead to preterm infants developing IVH. Therefore, strategies focused on antenatal management, such as routine corticosteroid administration and magnesium sulfate use; perinatal management, such as maternal transfer to a specialized center; and postnatal management, including pharmacological agent administration and circulatory management involving prevention of extreme blood pressure, hemodynamic significant patent ductus arteriosus management, and optimization of cardiac function, can lower the likelihood of IVH development in preterm infants. Incorporating neuroprotective care bundles into routine care for such infants may also reduce the likelihood of IVH development. The findings regarding the pathogenesis of IVH further indicate that cerebrovascular status and systemic hemodynamic changes must be analyzed and monitored in preterm infants and that individualized management strategies must be developed with consideration of the risk factors for and physiological status of each preterm infant.

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참고문헌

  1. Al-Matary A, Abu Shaheen A, Abozaid S : Use of prophylactic indomethacin in preterm infants: a systematic review and meta-analysis. Front Pediatr 10 : 760029,
  2. Alotaibi WSM, Alsaif NS, Ahmed IA, Mahmoud AF, Ali K, Hammad A, et al. : Reduction of severe intraventricular hemorrhage, a tertiary single-center experience: incidence trends, associated risk factors, and hospital policy. Childs Nerv Syst 36 : 2971-2979, 2020 https://doi.org/10.1007/s00381-020-04621-7
  3. Altaany D, Natarajan G, Gupta D, Zidan M, Chawla S : Severe intraventricular hemorrhage in extremely premature infants: are high carbon dioxide pressure or fluctuations the culprit? Am J Perinatol 32 : 839-844, 2015 https://doi.org/10.1055/s-0034-1543950
  4. Aly S, El-Dib M, Lu Z, El Tatawy S, Mohamed M, Aly H : Factors affecting cerebrovascular reactivity to CO2 in premature infants. J Perinat Med 47 : 979-985, 2019 https://doi.org/10.1515/jpm-2019-0031
  5. American College of Obstetricians and Gynecologists; Society for Maternal-Fetal Medicine : Obstetric care consensus No. 6: periviable birth. Obstet Gynecol 130 : e187-e199, 2017 https://doi.org/10.1097/AOG.0000000000002352
  6. Auerbach A, Eventov-Friedman S, Arad I, Peleg O, Bdolah-Abram T, Bar-Oz B, et al. : Long duration of hyperglycemia in the first 96 hours of life is associated with severe intraventricular hemorrhage in preterm infants. J Pediatr 163 : 388-393, 2013 https://doi.org/10.1016/j.jpeds.2013.01.051
  7. Ayed M, Ahmed J, More K, Ayed A, Husain H, AlQurashi A, et al. : Antenatal magnesium sulfate for preterm neuroprotection: a single-center experience from Kuwait Tertiary NICU. Biomed Hub 7 : 80-87,
  8. Balasubramanian H, Ananthan A, Jain V, Rao SC, Kabra N : Umbilical cord milking in preterm infants: a systematic review and meta-analysis. Arch Dis Child Fetal Neonatal Ed 105 : 572-580, 2020 https://doi.org/10.1136/archdischild-2019-318627
  9. Bansal V, Desai A : Efficacy of antenatal magnesium sulfate for neuroprotection in extreme prematurity: a comparative observational study. J Obstet Gynaecol India 72 : 36-47,
  10. Bates S, Odd D, Luyt K, Mannix P, Wach R, Evans D, et al. : Superior vena cava flow and intraventricular haemorrhage in extremely preterm infants. J Matern Fetal Neonatal Med 29 : 1581-1587, 2016 https://doi.org/10.3109/14767058.2015.1054805
  11. Baumgartner S, Olischar M, Wald M, Werther T, Berger A, Waldhor T, et al. : Left ventricular pumping during the transition-adaptation sequence in preterm infants: impact of the patent ductus arteriosus. Pediatr Res 83 : 1016-1023, 2018
  12. Borna H, Rad SM, Borna S, Mohseni SM : Incidence of and risk factors for birth trauma in Iran. Taiwan J Obstet Gynecol 49 : 170-173, 2010 https://doi.org/10.1016/S1028-4559(10)60036-8
  13. Brunner B, Hoeck M, Schermer E, Streif W, Kiechl-Kohlendorfer U : Patent ductus arteriosus, low platelets, cyclooxygenase inhibitors, and intraventricular hemorrhage in very low birth weight preterm infants. J Pediatr 163 : 23-28, 2013 https://doi.org/10.1016/j.jpeds.2012.12.035
  14. Castrodale V, Rinehart S : The golden hour: improving the stabilization of the very low birth-weight infant. Adv Neonatal Care 14 : 9-14; quiz 15-16, 2014 https://doi.org/10.1097/ANC.0000000000000056
  15. Cayabyab R, McLean CW, Seri I : Definition of hypotension and assessment of hemodynamics in the preterm neonate. J Perinatol 29 Suppl 2 : S58-S62, 2009 https://doi.org/10.1038/jp.2009.29
  16. Chen X, Li X, Chang Y, Li W, Cui H : Effect and safety of timing of cord clamping on neonatal hematocrit values and clinical outcomes in term infants: a randomized controlled trial. J Perinatol 38 : 251-257, 2018 https://doi.org/10.1038/s41372-017-0001-y
  17. Chock VY, Ramamoorthy C, Van Meurs KP : Cerebral autoregulation in neonates with a hemodynamically significant patent ductus arteriosus. J Pediatr 160 : 936-942, 2012 https://doi.org/10.1016/j.jpeds.2011.11.054
  18. Christian EA, Jin DL, Attenello F, Wen T, Cen S, Mack WJ, et al. : Trends in hospitalization of preterm infants with intraventricular hemorrhage and hydrocephalus in the United States, 2000-2010. J Neurosurg Pediatr 17 : 260-269, 2016 https://doi.org/10.3171/2015.7.PEDS15140
  19. Ciccone MM, Scicchitano P, Zito A, Gesualdo M, Sassara M, Calderoni G, et al. : Different functional cardiac characteristics observed in term/preterm neonates by echocardiography and tissue doppler imaging. Early Hum Dev 87 : 555-558, 2011
  20. Cools F, Offringa M, Askie LM : Elective high frequency oscillatory ventilation versus conventional ventilation for acute pulmonary dysfunction in preterm infants. Cochrane Database Syst Rev (3) : CD000104, 2015
  21. Costa STB, Costa P, Graca AM, Abrantes M; Portuguese National Registry of very low birth weight infants : Delivery mode and neurological complications in very low birth weight infants. Am J Perinatol, 2022 [Epub ahead of print]
  22. da Costa CS, Czosnyka M, Smielewski P, Austin T : Optimal mean arterial blood pressure in extremely preterm infants within the first 24 hours of life. J Pediatr 203 : 242-248, 2018 https://doi.org/10.1016/j.jpeds.2018.07.096
  23. de Bijl-Marcus K, Brouwer AJ, De Vries LS, Groenendaal F, Wezel-Meijler GV : Neonatal care bundles are associated with a reduction in the incidence of intraventricular haemorrhage in preterm infants: a multicentre cohort study. Arch Dis Child Fetal Neonatal Ed 105 : 419-424, 2020 https://doi.org/10.1136/archdischild-2018-316692
  24. de Figueiredo Vinagre LE, de Siqueira Caldas JP, Martins Marba ST, Procianoy RS, de Cassia Silveira R, Santiago Rego MA, et al. : Temporal trends in intraventricular hemorrhage in preterm infants: a Brazilian multicenter cohort. Eur J Paediatr Neurol 39 : 65-73, 2022 https://doi.org/10.1016/j.ejpn.2022.05.003
  25. Dempsey EM : What should we do about low blood pressure in preterm infants. Neonatology 111 : 402-407, 2017 https://doi.org/10.1159/000460603
  26. Dempsey EM, Al Hazzani F, Barrington KJ : Permissive hypotension in the extremely low birthweight infant with signs of good perfusion. Arch Dis Child Fetal Neonatal Ed 94 : F241-244, 2009 https://doi.org/10.1136/adc.2007.124263
  27. Dempsey EM, Barrington KJ : Diagnostic criteria and therapeutic interventions for the hypotensive very low birth weight infant. J Perinatol 26 : 677-681, 2006 https://doi.org/10.1038/sj.jp.7211579
  28. Dix L, Molenschot M, Breur J, de Vries W, Vijlbrief D, Groenendaal F, et al. : Cerebral oxygenation and echocardiographic parameters in preterm neonates with a patent ductus arteriosus: an observational study. Arch Dis Child Fetal Neonatal Ed 101 : F520-F526, 2016 https://doi.org/10.1136/archdischild-2015-309192
  29. Dzietko M, Schulz S, Preuss M, Haertel C, Stein A, Felderhoff-Mueser U, et al. : Apolipoprotein E gene polymorphisms and intraventricular haemorrhage in infants born preterm: a large prospective multicentre cohort study. Dev Med Child Neurol 61 : 337-342, 2019 https://doi.org/10.1111/dmcn.13987
  30. Egesa WI, Odoch S, Odong RJ, Nakalema G, Asiimwe D, Ekuk E, et al. : Germinal matrix-intraventricular hemorrhage: a tale of preterm infants. Int J Pediatr 2021 : 6622598, 2021
  31. Erickson SJ, Grauaug A, Gurrin L, Swaminathan M : Hypocarbia in the ventilated preterm infant and its effect on intraventricular haemorrhage and bronchopulmonary dysplasia. J Paediatr Child Health 38 : 560-562, 2002 https://doi.org/10.1046/j.1440-1754.2002.00041.x
  32. Evans N, Kluckow M : Early ductal shunting and intraventricular haemorrhage in ventilated preterm infants. Arch Dis Child Fetal Neonatal Ed 75 : F183-186, 1996 https://doi.org/10.1136/fn.75.3.F183
  33. Fabres J, Carlo WA, Phillips V, Howard G, Ambalavanan N : Both extremes of arterial carbon dioxide pressure and the magnitude of fluctuations in arterial carbon dioxide pressure are associated with severe intraventricular hemorrhage in preterm infants. Pediatrics 119 : 299-305, 2007 https://doi.org/10.1542/peds.2006-2434
  34. Ferreira DM, Girao ALA, AVS ES, Chaves EMC, de Almeida PC, Freire VS, et al. : Application of a bundle in the prevention of peri-intraventricular hemorrhage in preterm newborns. J Perinat Neonatal Nurs 34 : E5-E11, 2020 https://doi.org/10.1097/JPN.0000000000000482
  35. Fogarty M, Osborn DA, Askie L, Seidler AL, Hunter K, Lui K, et al. : Delayed vs early umbilical cord clamping for preterm infants: a systematic review and meta-analysis. Am J Obstet Gynecol 218 : 1-18, 2018 https://doi.org/10.1016/j.ajog.2017.10.231
  36. Fortmann I, Mertens L, Boeckel H, Gruttner B, Humberg A, Astiz M, et al. : A timely administration of antenatal steroids is highly protective against intraventricular hemorrhage: an observational multicenter cohort study of very low birth weight infants. Front Pediatr 10 : 721355, 2022
  37. Friedman WF : The intrinsic physiologic properties of the developing heart. Prog Cardiovasc Dis 15 : 87-111, 1972 https://doi.org/10.1016/0033-0620(72)90006-0
  38. Gamaleldin I, Harding D, Siassakos D, Draycott T, Odd D : Significant intraventricular hemorrhage is more likely in very preterm infants born by vaginal delivery: a multi-centre retrospective cohort study. J Matern Fetal Neonatal Med 32 : 477-482, 2019 https://doi.org/10.1080/14767058.2017.1383980
  39. Gross M, Engel C, Trotter A : Evaluating the effect of a neonatal care bundle for the prevention of intraventricular hemorrhage in preterm infants. Children (Basel) 8 : 257, 2021
  40. Hamrick SEG, Sallmon H, Rose AT, Porras D, Shelton EL, Reese J, et al. : Patent ductus arteriosus of the preterm infant. Pediatrics 146 : e20201209, 2020
  41. Hatfield LA, Murphy N, Karp K, Polomano RC : A systematic review of behavioral and environmental interventions for procedural pain management in preterm infants. J Pediatr Nurs 44 : 22-30, 2019 https://doi.org/10.1016/j.pedn.2018.10.004
  42. Helwich E, Rutkowska M, Bokiniec R, Gulczynska E, Hozejowski R : Intraventricular hemorrhage in premature infants with Respiratory Distress Syndrome treated with surfactant: incidence and risk factors in the prospective cohort study. Dev Period Med 21 : 328-335, 2017
  43. Hemmati F, Sharma D, Namavar Jahromi B, Salarian L, Farahbakhsh N : Delayed cord clamping for prevention of intraventricular hemorrhage in preterm neonates: a randomized control trial. J Matern Fetal Neonatal Med 35 : 3633-3639, 2022 https://doi.org/10.1080/14767058.2020.1836148
  44. Hubner ME, Ramirez R, Burgos J, Dominguez A, Tapia JL : Mode of delivery and antenatal steroids and their association with survival and severe intraventricular hemorrhage in very low birth weight infants. J Perinatol 36 : 832-836, 2016 https://doi.org/10.1038/jp.2016.78
  45. Humberg A, Hartel C, Paul P, Hanke K, Bossung V, Hartz A, et al. : Delivery mode and intraventricular hemorrhage risk in very-low-birth-weight infants: observational data of the German Neonatal Network. Eur J Obstet Gynecol Reprod Biol 212 : 144-149, 2017 https://doi.org/10.1016/j.ejogrb.2017.03.032
  46. Ikeda T, Ito Y, Mikami R, Matsuo K, Kawamura N, Yamoto A, et al. : Fluctuations in internal cerebral vein and central side veins of preterm infants. Pediatr Int 63 : 1319-1326, 2021 https://doi.org/10.1111/ped.14638
  47. Jelin AC, Zlatnik MG, Kuppermann M, Gregorich SE, Nakagawa S, Clyman R : Clamp late and maintain perfusion (CLAMP) policy: delayed cord clamping in preterm infants. J Matern Fetal Neonatal Med 29 : 1705-1709, 2016 https://doi.org/10.3109/14767058.2015.1061496
  48. Jim WT, Chiu NC, Chen MR, Hung HY, Kao HA, Hsu CH, et al. : Cerebral hemodynamic change and intraventricular hemorrhage in very low birth weight infants with patent ductus arteriosus. Ultrasound Med Biol 31 : 197-202, 2005 https://doi.org/10.1016/j.ultrasmedbio.2004.10.006
  49. Kaiser JR, Gauss CH, Pont MM, Williams DK : Hypercapnia during the first 3 days of life is associated with severe intraventricular hemorrhage in very low birth weight infants. J Perinatol 26 : 279-285, 2006 https://doi.org/10.1038/sj.jp.7211492
  50. Kalani M, Shariat M, Khalesi N, Farahani Z, Ahmadi S : A comparison of early ibuprofen and indomethacin administration to prevent intraventricular hemorrhage among preterm infants. Acta Med Iran 54 : 788-792, 2016
  51. Karagol BS, Calisici E, Zeybek C, Unay B, Yuksel S : The impact of initial hematocrit values after birth on peri-/intraventricular hemorrhage in extremely low birth weight neonates. Childs Nerv Syst 38 : 109-114, 2022 https://doi.org/10.1007/s00381-021-05398-z
  52. Katheria AC, Szychowski JM, Essers J, Mendler MR, Dempsey EM, Schmolzer GM, et al. : Early cardiac and cerebral hemodynamics with umbilical cord milking compared with delayed cord clamping in infants born preterm. J Pediatr 223 : 51-56.e1, 2020 https://doi.org/10.1016/j.jpeds.2020.04.010
  53. Kc A, Malqvist M, Rana N, Ranneberg LJ, Andersson O : Effect of timing of umbilical cord clamping on anaemia at 8 and 12 months and later neurodevelopment in late pre-term and term infants; a facility-based, randomized-controlled trial in Nepal. BMC Pediatr 16 : 35, 2016
  54. Khanafer-Larocque I, Soraisham A, Stritzke A, Al Awad E, Thomas S, Murthy P, et al. : Intraventricular hemorrhage: risk factors and association with patent ductus arteriosus treatment in extremely preterm neonates. Front Pediatr 7 : 408, 2019
  55. Klingenberg C, Wheeler KI, McCallion N, Morley CJ, Davis PG : Volume-targeted versus pressure-limited ventilation in neonates. Cochrane Database Syst Rev 10 : CD003666, 2017
  56. Kluckow M : The pathophysiology of low systemic blood flow in the preterm infant. Front Pediatr 6 : 29, 2018
  57. Kluckow M, Evans N : Low superior vena cava flow and intraventricular haemorrhage in preterm infants. Arch Dis Child Fetal Neonatal Ed 82 : F188-194, 2000 https://doi.org/10.1136/fn.82.3.F188
  58. Kochan M, Leonardi B, Firestine A, McPadden J, Cobb D, Shah TA, et al. : Elevated midline head positioning of extremely low birth weight infants: effects on cardiopulmonary function and the incidence of periventricular-intraventricular hemorrhage. J Perinatol 39 : 54-62, 2019 https://doi.org/10.1038/s41372-018-0261-1
  59. Kooi EMW, Richter AE : Cerebral autoregulation in sick infants: current insights. Clin Perinatol 47 : 449-467, 2020 https://doi.org/10.1016/j.clp.2020.05.003
  60. Kooi EMW, Verhagen EA, Elting JWJ, Czosnyka M, Austin T, Wong FY, et al. : Measuring cerebrovascular autoregulation in preterm infants using near-infrared spectroscopy: an overview of the literature. Expert Rev Neurother 17 : 801-818, 2017
  61. Kumar Nair PA, Pai MG, Gazal HA, Da Costa DE, Al Khusaiby SM : Indomethacin prophylaxis for intraventricular hemorrhage in very low birth weight babies. Indian Pediatr 41 : 551-558, 2004
  62. Leviton A, Fenton T, Kuban KC, Pagano M : Labor and delivery characteristics and the risk of germinal matrix hemorrhage in low birth weight infants. J Child Neurol 6 : 35-40, 1991 https://doi.org/10.1177/088307389100600107
  63. Lightburn MH, Gauss CH, Williams DK, Kaiser JR : Cerebral blood flow velocities in extremely low birth weight infants with hypotension and infants with normal blood pressure. J Pediatr 154 : 824-828, 2009 https://doi.org/10.1016/j.jpeds.2009.01.006
  64. Ljustina S, Berisavac, II, Berisavac M, Kovacevic-Vukolic L, Velickovic-Aleksic V, Markovic N : Analysis of intracranial hemorrhage grade in preterm singleton pregnancies delivered vaginally or by cesarean section. Vojnosanit Pregl 70 : 255-258, 2013 https://doi.org/10.2298/VSP1303255L
  65. Lou HC, Lassen NA, Friis-Hansen B : Impaired autoregulation of cerebral blood flow in the distressed newborn infant. J Pediatr 94 : 118-121, 1979 https://doi.org/10.1016/S0022-3476(79)80373-X
  66. Luca A, Vinturache A, Ilea C, Avasiloaiei A, Paduraru L, Carauleanu A, et al. : Birth trauma in preterm spontaneous vaginal and cesarean section deliveries: a 10-years retrospective study. PLoS One 17 : e0275726, 2022
  67. Martini S, Czosnyka M, Smielewski P, Iommi M, Galletti S, Vitali F, et al. : Clinical determinants of cerebrovascular reactivity in very preterm infants during the transitional period. Pediatr Res 92 : 135-141, 2022 https://doi.org/10.1038/s41390-022-02090-z
  68. McGoldrick E, Stewart F, Parker R, Dalziel SR : Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst Rev 12 : CD004454, 2020
  69. McLendon D, Check J, Carteaux P, Michael L, Moehring J, Secrest JW, et al. : Implementation of potentially better practices for the prevention of brain hemorrhage and ischemic brain injury in very low birth weight infants. Pediatrics 111(4 Pt 2) : e497-503, 2003 https://doi.org/10.1542/peds.111.SE1.e497
  70. Ment LR, Oh W, Ehrenkranz RA, Philip AG, Duncan CC, Makuch RW : Antenatal steroids, delivery mode, and intraventricular hemorrhage in preterm infants. Am J Obstet Gynecol 172 : 795-800, 1995 https://doi.org/10.1016/0002-9378(95)90001-2
  71. Ment LR, Oh W, Ehrenkranz RA, Philip AG, Vohr B, Allan W, et al. : Low-dose indomethacin and prevention of intraventricular hemorrhage: a multicenter randomized trial. Pediatrics 93 : 543-550, 1994 https://doi.org/10.1542/peds.93.4.543
  72. Miller CJ, Prusakov P, Magers J, Speaks S, Sacic H, Escobar K, et al. : Effects of prophylactic indomethacin on intraventricular hemorrhage and adverse outcomes in neonatal intensive care unit. J Perinatol 42 : 1644-1648, 2022 https://doi.org/10.1038/s41372-022-01441-2
  73. Mitra S, Florez ID, Tamayo ME, Mbuagbaw L, Vanniyasingam T, Veroniki AA, et al. : Association of placebo, indomethacin, ibuprofen, and acetaminophen with closure of hemodynamically significant patent ductus arteriosus in preterm infants: a systematic review and meta-analysis. JAMA 319 : 1221-1238, 2018 https://doi.org/10.1001/jama.2018.1896
  74. Mittendorf R, Besinger R, Santillan M, Gianopoulos J : When used in the circumstance of preterm labor, is there a paradoxical effect of varying exposures to magnesium sulfate (MgSO4) on the developing human brain? Am J Obstet Gynecol 193 (6 Suppl) : S65, 2005
  75. Mittendorf R, Dambrosia J, Dammann O, Pryde PG, Lee KS, Ben-Ami TE, et al. : Association between maternal serum ionized magnesium levels at delivery and neonatal intraventricular hemorrhage. J Pediatr 140 : 540-546, 2002 https://doi.org/10.1067/mpd.2002.123283
  76. Moriette G, Paris-Llado J, Walti H, Escande B, Magny JF, Cambonie G, et al. : Prospective randomized multicenter comparison of high-frequency oscillatory ventilation and conventional ventilation in preterm infants of less than 30 weeks with respiratory distress syndrome. Pediatrics 107 : 363-372, 2001 https://doi.org/10.1542/peds.107.2.363
  77. Mullaart RA, Hopman JC, Rotteveel JJ, Stoelinga GB, De Haan AF, Daniels O : Cerebral blood flow velocity and pulsation in neonatal respiratory distress syndrome and periventricular hemorrhage. Pediatr Neurol 16 : 118-125, 1997 https://doi.org/10.1016/S0887-8994(96)00291-3
  78. Noone MA, Sellwood M, Meek JH, Wyatt JS : Postnatal adaptation of cerebral blood flow using near infrared spectroscopy in extremely preterm infants undergoing high-frequency oscillatory ventilation. Acta Paediatr 92 : 1079-1084, 2003 https://doi.org/10.1111/j.1651-2227.2003.tb02581.x
  79. Noori S, Seri I : Hemodynamic antecedents of peri/intraventricular hemorrhage in very preterm neonates. Semin Fetal Neonatal Med 20 : 232-237, 2015 https://doi.org/10.1016/j.siny.2015.02.004
  80. Ohlsson A, Shah PS : Paracetamol (acetaminophen) for patent ductus arteriosus in preterm or low birth weight infants. Cochrane Database Syst Rev 4 : CD010061, 2018
  81. Okulu E, Haskologlu S, Guloglu D, Kostekci E, Erdeve O, Atasay B, et al. : Effects of umbilical cord management strategies on stem cell transfusion, delivery room adaptation, and cerebral oxygenation in term and late preterm infants. Front Pediatr 10 : 838444, 2022
  82. Pan I, Shah PA, Singh J, Kelly KN, Bondi DS : Comparison of neonatal outcomes with and without prophylaxis with indomethacin in premature neonates. J Pediatr Pharmacol Ther 26 : 478-483, 2021 https://doi.org/10.5863/1551-6776-26.5.478
  83. Panerai RB, Kelsall AW, Rennie JM, Evans DH : Cerebral autoregulation dynamics in premature newborns. Stroke 26 : 74-80, 1995 https://doi.org/10.1161/01.STR.26.1.74
  84. Parker LA : Part 1: early recognition and treatment of birth trauma: injuries to the head and face. Adv Neonatal Care 5 : 288-297; quiz 298-300, 2005 https://doi.org/10.1016/j.adnc.2005.09.001
  85. Persad N, Kelly E, Amaral N, Neish A, Cheng C, Fan CS, et al. : Impact of a "Brain Protection Bundle" in reducing severe intraventricular hemorrhage in preterm infants <30 weeks GA: a retrospective single centre study. Children (Basel) 8 : 983, 2021
  86. Pinto Cardoso G, Houivet E, Marchand-Martin L, Kayem G, Sentilhes L, Ancel PY, et al. : Association of intraventricular hemorrhage and death with tocolytic exposure in preterm infants. JAMA Netw Open 1 : e182355, 2018
  87. Pishva N, Parsa G, Saki F, Saki M, Saki MR : Intraventricular hemorrhage in premature infants and its association with pneumothorax. Acta Med Iran 50 : 473-476, 2012
  88. Piteaud I, Abdennour L, Icke C, Stany I, Lescot T, Puybasset L : Superior vena cava syndrome: cause of secondary raise of intracranial pressure after traumatic brain injury. Ann Fr Anesth Reanim 27 : 850-853, 2008 https://doi.org/10.1016/j.annfar.2008.08.002
  89. Poryo M, Boeckh JC, Gortner L, Zemlin M, Duppre P, Ebrahimi-Fakhari D, et al. : Ante-, peri- and postnatal factors associated with intraventricular hemorrhage in very premature infants. Early Hum Dev 116 : 1-8, 2018 https://doi.org/10.1016/j.earlhumdev.2017.08.010
  90. Rahman S, Ullah M, Ali A, Afridi N, Bashir H, Amjad Z, et al. : Fetal outcomes in preterm cesarean sections. Cureus 14 : e27607, 2022
  91. Raybaud C : Normal and abnormal embryology and development of the intracranial vascular system. Neurosurg Clin N Am 21 : 399-426, 2010 https://doi.org/10.1016/j.nec.2010.03.011
  92. Rhee CJ, Fraser CD 3rd, Kibler K, Easley RB, Andropoulos DB, Czosnyka M, et al. : The ontogeny of cerebrovascular pressure autoregulation in premature infants. J Perinatol 34 : 926-931, 2014 https://doi.org/10.1038/jp.2014.122
  93. Riskin A, Riskin-Mashiah S, Bader D, Kugelman A, Lerner-Geva L, Boyko V, et al. : Delivery mode and severe intraventricular hemorrhage in single, very low birth weight, vertex infants. Obstet Gynecol 112 : 21-28, 2008 https://doi.org/10.1097/AOG.0b013e31817cfdf1
  94. Roze JC, Cambonie G, Marchand-Martin L, Gournay V, Durrmeyer X, Durox M, et al. : Association between early screening for patent ductus arteriosus and in-hospital mortality among extremely preterm infants. JAMA 313 : 2441-2448, 2015 https://doi.org/10.1001/jama.2015.6734
  95. Sankar MN, Bhombal S, Benitz WE : PDA: to treat or not to treat. Congenit Heart Dis 14 : 46-51, 2019 https://doi.org/10.1111/chd.12708
  96. Schreiner C, Suter S, Watzka M, Hertfelder HJ, Schreiner F, Oldenburg J, et al. : Genetic variants of the vitamin K dependent coagulation system and intraventricular hemorrhage in preterm infants. BMC Pediatr 14 : 219, 2014
  97. Schulz G, Keller E, Haensse D, Arlettaz R, Bucher HU, Fauchere JC : Slow blood sampling from an umbilical artery catheter prevents a decrease in cerebral oxygenation in the preterm newborn. Pediatrics 111 : e73-76, 2003 https://doi.org/10.1542/peds.111.1.e73
  98. Semberova J, Sirc J, Miletin J, Kucera J, Berka I, Sebkova S, et al. : Spontaneous closure of patent ductus arteriosus in infants ≤1500 g. Pediatrics 140 : e20164258, 2017
  99. Seri I : Management of hypotension and low systemic blood flow in the very low birth weight neonate during the first postnatal week. J Perinatol 26 Suppl 1 : S8-S13; discussion S22-S23, 2006 https://doi.org/10.1038/sj.jp.7211464
  100. Shah V, Hodgson K, Seshia M, Dunn M, Schmolzer GM : Golden hour management practices for infants <32 weeks gestational age in Canada. Paediatr Child Health 23 : e70-e76, 2018 https://doi.org/10.1093/pch/pxx175
  101. Soul JS, Hammer PE, Tsuji M, Saul JP, Bassan H, Limperopoulos C, et al. : Fluctuating pressure-passivity is common in the cerebral circulation of sick premature infants. Pediatr Res 61 : 467-473, 2007 https://doi.org/10.1203/pdr.0b013e31803237f6
  102. Su BH, Lin HY, Chiu HY, Tsai ML, Chen YT, Lu IC : Therapeutic strategy of patent ductus arteriosus in extremely preterm infants. Pediatr Neonatol 61 : 133-141, 2020 https://doi.org/10.1016/j.pedneo.2019.10.002
  103. Szpecht D, Al-Saad SR, Karbowski LM, Kosik K, Kurzawinska G, Szymankiewicz M, et al. : Role of fibronectin-1 polymorphism genes with the pathogenesis of intraventricular hemorrhage in preterm infants. Childs Nerv Syst 36 : 1729-1736, 2020 https://doi.org/10.1007/s00381-020-04598-3
  104. Szpecht D, Gadzinowski J, Seremak-Mrozikiewicz A, Kurzawinska G, Drews K, Szymankiewicz M : The significance of polymorphisms in genes encoding Il-1β, Il-6, TNFα, and Il-1RN in the pathogenesis of intraventricular hemorrhage in preterm infants. Childs Nerv Syst 33 : 1905-1916, 2017 https://doi.org/10.1007/s00381-017-3458-2
  105. Szpecht D, Gadzinowski J, Seremak-Mrozikiewicz A, Kurzawinska G, Szymankiewicz M : Role of endothelial nitric oxide synthase and endothelin-1 polymorphism genes with the pathogenesis of intraventricular hemorrhage in preterm infants. Sci Rep 7 : 42541, 2017
  106. Takahashi Y, Harada K, Kishkurno S, Arai H, Ishida A, Takada G : Postnatal left ventricular contractility in very low birth weight infants. Pediatr Cardiol 18 : 112-117, 1997 https://doi.org/10.1007/s002469900127
  107. Thewissen L, Naulaers G, Hendrikx D, Caicedo A, Barrington K, Boylan G, et al. : Cerebral oxygen saturation and autoregulation during hypotension in extremely preterm infants. Pediatr Res 90 : 373-380, 2021 https://doi.org/10.1038/s41390-021-01483-w
  108. Thornburg CD, Erickson SW, Page GP, Clark EAS, DeAngelis MM, Hartnett ME, et al. : Genetic predictors of severe intraventricular hemorrhage in extremely low-birthweight infants. J Perinatol 41 : 286-294, 2021 https://doi.org/10.1038/s41372-020-00821-w
  109. Toledo JD, Rodilla S, Perez-Iranzo A, Delgado A, Maazouzi Y, Vento M : Umbilical cord milking reduces the risk of intraventricular hemorrhage in preterm infants born before 32 weeks of gestation. J Perinatol 39 : 547-553, 2019 https://doi.org/10.1038/s41372-019-0329-6
  110. Tomotaki S, Iwanaga K, Hanaoka S, Tomotaki H, Matsukura T, Niwa F, et al. : Antenatal glucocorticoids reduce the incidence of refractory hypotension in low birthweight infants during the early neonatal period, but do not affect it beyond this time. Am J Perinatol 38 : 1057-1061, 2021 https://doi.org/10.1055/s-0040-1701608
  111. Toyoshima K, Kawataki M, Ohyama M, Shibasaki J, Yamaguchi N, Hoshino R, et al. : Tailor-made circulatory management based on the stress-velocity relationship in preterm infants. J Formos Med Assoc 112 : 510-517, 2013 https://doi.org/10.1016/j.jfma.2013.02.011
  112. Tsuji M, Saul JP, du Plessis A, Eichenwald E, Sobh J, Crocker R, et al. : Cerebral intravascular oxygenation correlates with mean arterial pressure in critically ill premature infants. Pediatrics 106 : 625-632, 2000 https://doi.org/10.1542/peds.106.4.625
  113. van Beek PE, Groenendaal F, Broeders L, Dijk PH, Dijkman KP, van den Dungen FAM, et al. : Survival and causes of death in extremely preterm infants in the Netherlands. Arch Dis Child Fetal Neonatal Ed 106 : 251-257, 2021 https://doi.org/10.1136/archdischild-2020-318978
  114. van Bel F, Mintzer JP : Monitoring cerebral oxygenation of the immature brain: a neuroprotective strategy? Pediatr Res 84 : 159-164, 2018 https://doi.org/10.1038/s41390-018-0026-8
  115. van der Laan ME, Roofthooft MT, Fries MW, Berger RM, Schat TE, van Zoonen AG, et al. : A hemodynamically significant patent ductus arteriosus does not affect cerebral or renal tissue oxygenation in preterm infants. Neonatology 110 : 141-147, 2016 https://doi.org/10.1159/000445101
  116. Verma PK, Panerai RB, Rennie JM, Evans DH : Grading of cerebral autoregulation in preterm and term neonates. Pediatr Neurol 23 : 236-242, 2000 https://doi.org/10.1016/S0887-8994(00)00184-3
  117. Vesoulis ZA, Flower AA, Zanelli S, Rambhia A, Abubakar M, Whitehead HV, et al. : Blood pressure extremes and severe IVH in preterm infants. Pediatr Res 87 : 69-73, 2020 https://doi.org/10.1038/s41390-019-0585-3
  118. Vesoulis ZA, Liao SM, Mathur AM : Gestational age-dependent relationship between cerebral oxygen extraction and blood pressure. Pediatr Res 82 : 934-939, 2017 https://doi.org/10.1038/pr.2017.196
  119. Vinukonda G, Dummula K, Malik S, Hu F, Thompson CI, Csiszar A, et al. : Effect of prenatal glucocorticoids on cerebral vasculature of the developing brain. Stroke 41 : 1766-1773, 2010 https://doi.org/10.1161/STROKEAHA.110.588400
  120. Wardle SP, Yoxall CW, Weindling AM : Determinants of cerebral fractional oxygen extraction using near infrared spectroscopy in preterm neonates. J Cereb Blood Flow Metab 20 : 272-279, 2000 https://doi.org/10.1097/00004647-200002000-00008
  121. Wei JC, Catalano R, Profit J, Gould JB, Lee HC : Impact of antenatal steroids on intraventricular hemorrhage in very-low-birth weight infants. J Perinatol 36 : 352-356, 2016 https://doi.org/10.1038/jp.2016.38
  122. Wolf HT, Weber T, Schmidt S, Norman M, Varendi H, Piedvache A, et al. : Mode of delivery and adverse short- and long-term outcomes in vertex-presenting very preterm born infants: a European population-based prospective cohort study. J Perinat Med 49 : 923-931, 2021 https://doi.org/10.1515/jpm-2020-0468
  123. Wong FY, Leung TS, Austin T, Wilkinson M, Meek JH, Wyatt JS, et al. : Impaired autoregulation in preterm infants identified by using spatially resolved spectroscopy. Pediatrics 121 : e604-e611, 2008 https://doi.org/10.1542/peds.2007-1487
  124. Xu H, Hu F, Sado Y, Ninomiya Y, Borza DB, Ungvari Z, et al. : Maturational changes in laminin, fibronectin, collagen IV, and perlecan in germinal matrix, cortex, and white matter and effect of betamethasone. J Neurosci Res 86 : 1482-1500, 2008 https://doi.org/10.1002/jnr.21618
  125. Yao SL, Smit E, Odd D : The effectiveness of interventions to prevent intraventricular haemorrhage in premature infants: a systematic review and network meta-analysis. J Neonatal Perinatal Med 16 : 5-20, 2023
  126. Committee Opinion No. 455: magnesium sulfate before anticipated preterm birth for neuroprotection. Obstet Gynecol 115 : 669-671, 2010 https://doi.org/10.1097/AOG.0b013e3181d4ffa5
  127. Committee Opinion No 652: magnesium sulfate use in obstetrics. Obstet Gynecol 127 : e52-e53, 2016 https://doi.org/10.1097/AOG.0000000000001267