Abstract

Stress is a major factor for a risk of cerebrovascular catastrophes. Studying of mechanisms underlying stress-related brain-injures in neonates is crucial for development of strategy to prevent of neonatal stroke. Here, using a model of sound-stress-induced intracranial hemorrhages in newborn rats and optical methods, we found that cerebral veins are more sensitive to the deleterious effect of stress than arteries and microvessels. The development of venous insufficiency with decreased blood outflow from the brain accompanied by hypoxia, reduction of complexity of venous blood flow and high production of beta-arrestin-1 are possible mechanisms responsible for a risk of neonatal hemorrhagic stroke.

© 2015 Optical Society of America

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2015 (4)

S. M. Kazmi, E. Faraji, M. A. Davis, Y. Y. Huang, X. J. Zhang, and A. K. Dunn, “Flux or speed? Examining speckle contrast imaging of vascular flows,” Biomed. Opt. Express 6(7), 2588–2608 (2015).
[Crossref] [PubMed]

K. Kosar and S. J. Kirkpatrick, “Effects of combined scattering and absorption coefficients on laser speckle contrast imaging values”, Proc. SPIE 9322, 93220U (2015).

N. Liu, X. Cui, D. M. Bryant, G. H. Glover, and A. L. Reiss, “Inferring deep-brain activity from cortical activity using functional near-infrared spectroscopy,” Biomed. Opt. Express 6(3), 1074–1089 (2015).
[Crossref] [PubMed]

S. C. Tang, H. I. Jen, Y. H. Lin, C. S. Hung, W. J. Jou, P. W. Huang, J. S. Shieh, Y. L. Ho, D. M. Lai, A. Y. Wu, J. S. Jeng, and M. F. Chen, “Complexity of heart rate variability predicts outcome in intensive care unit admitted patients with acute stroke,” J. Neurol. Neurosurg. Psychiatry 86(1), 95–100 (2015).
[Crossref] [PubMed]

2014 (3)

J. You, C. Du, N. D. Volkow, and Y. Pan, “Optical coherence Doppler tomography for quantitative cerebral blood flow imaging,” Biomed. Opt. Express 5(9), 3217–3230 (2014).
[Crossref] [PubMed]

A. N. Pavlov, O. V. Semyachkina-Glushkovskaya, Y. Zhang, O. A. Bibikova, O. N. Pavlova, Q. Huang, D. Zhu, P. Li, V. V. Tuchin, and Q. Luo, “Multiresolution analysis of pathological changes in cerebral venous dynamics in newborn mice with intracranial hemorrhage: adrenorelated vasorelaxation,” Physiol. Meas. 35(10), 1983–1999 (2014).
[Crossref] [PubMed]

C. J. Bruno, L. A. Beslow, C. M. Witmer, A. Vossough, L. C. Jordan, S. Zelonis, D. J. Licht, R. N. Ichord, and S. E. Smith, “Haemorrhagic stroke in term and late preterm neonates,” Arch. Dis. Child. Fetal Neonatal Ed. 99(1), F48–F53 (2014).
[PubMed]

2013 (6)

A. Kirton and G. Deveber, “Life after perinatal stroke,” Stroke 44(11), 3265–3271 (2013).
[Crossref] [PubMed]

O. Semyachkina-Glushkovskaya, V. Lychagov, O. Bibikova, I. Semyachkin-Glushkovskiy, S. Sindeev, E. Zinchenko, M. Kassim, H. Braun, F. Al-Fatle, L. Al Hassani, and V. Tuchin, “The experimental study of stress-related pathological changes in cerebral venous blood flow in newborn rats assessed by DOCT,” J. Inn. Opt. Health Sci. 3(3), 1350023 (2013).

A. Pavlov, O. Semyachkina-Glushkovskaya, O. Pavlova, O. Bibikova, and J. Kurths, “Wavelet-analysis of gastric microcirculation in rats with ulcer bleedings,” Eur. Phys. J. Spec. Top. 222(10), 2705–2712 (2013).
[Crossref]

D. Briers, D. D. Duncan, E. Hirst, S. J. Kirkpatrick, M. Larsson, W. Steenbergen, T. Stromberg, and O. B. Thompson, “Laser speckle contrast imaging: theoretical and practical limitations,” J. Biomed. Opt. 18(6), 066018 (2013).
[Crossref] [PubMed]

J. M. Valdueza, F. Doepp, S. J. Schreiber, B. W. van Oosten, K. Schmierer, F. Paul, and M. P. Wattjes, “What went wrong? The flawed concept of cerebrospinal venous insufficiency,” J. Cereb. Blood Flow Metab. 33(5), 657–668 (2013).
[Crossref] [PubMed]

T. Alderliesten, P. M. Lemmers, J. J. Smarius, R. E. van de Vosse, W. Baerts, and F. van Bel, “Cerebral oxygenation, extraction, and autoregulation in very preterm infants who develop peri-intraventricular hemorrhage,” J. Pediatr. 162(4), 698–704 (2013).
[Crossref] [PubMed]

2012 (2)

C. L. MacLellan, R. Paquette, and F. Colbourne, “A critical appraisal of experimental intracerebral hemorrhage research,” J. Cereb. Blood Flow Metab. 32(4), 612–627 (2012).
[Crossref] [PubMed]

T. Takenouchi, E. Kasdorf, M. Engel, A. Grunebaum, and J. M. Perlman, “Changing pattern of perinatal brain injury in term infants in recent years,” Pediatr. Neurol. 46(2), 106–110 (2012).
[Crossref] [PubMed]

2011 (3)

A. Manaenko, H. Chen, J. H. Zhang, and J. Tang, “Comparison of different preclinical models of intracerebral hemorrhage,” Acta Neurochir. Suppl. (Wien) 111, 9–14 (2011).
[Crossref] [PubMed]

M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
[Crossref] [PubMed]

A. Michoulas, S. N. Basheer, E. H. Roland, K. Poskitt, S. Miller, and A. Hill, “The role of hypoxia-ischemia in term newborns with arterial stroke,” Pediatr. Neurol. 44(4), 254–258 (2011).
[Crossref] [PubMed]

2010 (3)

A. J. Brouwer, F. Groenendaal, C. Koopman, R. J. Nievelstein, S. K. Han, and L. S. de Vries, “Intracranial hemorrhage in full-term newborns: a hospital-based cohort study,” Neuroradiology 52(6), 567–576 (2010).
[Crossref] [PubMed]

P. Ballabh, “Intraventricular hemorrhage in premature infants: mechanism of disease,” Pediatr. Res. 67(1), 1–8 (2010).
[Crossref] [PubMed]

J. E. Lawn, K. Kerber, C. Enweronu-Laryea, and S. Cousens, “3.6 million neonatal deaths - what is progressing and what is not?” Semin. Perinatol. 34(6), 371–386 (2010).
[Crossref] [PubMed]

2009 (2)

S. N. Gupta, A. M. Kechli, and U. S. Kanamalla, “Intracranial hemorrhage in term newborns: management and outcomes,” Pediatr. Neurol. 40(1), 1–12 (2009).
[Crossref] [PubMed]

W. P. Riordan, P. R. Norris, J. M. Jenkins, and J. A. Morris., “Early loss of heart rate complexity predicts mortality regardless of mechanism, anatomic location, or severity of injury in 2178 trauma patients,” J. Surg. Res. 156(2), 283–289 (2009).
[Crossref] [PubMed]

2008 (1)

P. R. Norris, P. K. Stein, and J. A. Morris., “Reduced heart rate multiscale entropy predicts death in critical illness: a study of physiologic complexity in 285 trauma patients,” J. Crit. Care 23(3), 399–405 (2008).
[Crossref] [PubMed]

2007 (3)

T. Kiliç and A. Akakin, “Anatomy of cerebral veins and sinuses,” Front Neurol. Neurosci. 23, 4–15 (2007).
[Crossref] [PubMed]

L. C. Jordan and A. E. Hillis, “Hemorrhagic stroke in children,” Pediatr. Neurol. 36(2), 73–80 (2007).
[Crossref] [PubMed]

C. B. Looney, J. K. Smith, L. H. Merck, H. M. Wolfe, N. C. Chescheir, R. M. Hamer, and J. H. Gilmore, “Intracranial hemorrhage in asymptomatic neonates: prevalence on MR images and relationship to obstetric and neonatal risk factors,” Radiology 242(2), 535–541 (2007).
[Crossref] [PubMed]

2006 (3)

V. K. Paul, “The current state of newborn health in low income countries and the way forward,” Semin. Fetal Neonatal Med. 11(1), 7–14 (2006).
[Crossref] [PubMed]

T. K. Craft, N. Zhang, E. R. Glasper, P. D. Hurn, and A. C. Devries, “Neonatal factors influence adult stroke outcome,” Psychoneuroendocrinology 31(5), 601–613 (2006).
[Crossref] [PubMed]

H. Bassan, C. B. Benson, C. Limperopoulos, H. A. Feldman, S. A. Ringer, E. Veracruz, J. E. Stewart, J. S. Soul, D. N. Disalvo, J. J. Volpe, and A. J. du Plessis, “Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome,” Pediatrics 117(6), 2111–2118 (2006).
[Crossref] [PubMed]

2005 (2)

J. K. Lynch and C. J. Han, “Pediatric stroke: what do we know and what do we need to know?” Semin. Neurol. 25(4), 410–423 (2005).
[Crossref] [PubMed]

D. Wilson-Costello, H. Friedman, N. Minich, A. A. Fanaroff, and M. Hack, “Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s,” Pediatrics 115(4), 997–1003 (2005).
[Crossref] [PubMed]

2004 (2)

E. H. Whitby, P. D. Griffiths, S. Rutter, M. F. Smith, A. Sprigg, P. Ohadike, N. P. Davies, A. S. Rigby, and M. N. Paley, “Frequency and natural history of subdural haemorrhages in babies and relation to obstetric factors,” Lancet 363(9412), 846–851 (2004).
[Crossref] [PubMed]

M. S. Lombardi, E. van den Tweel, A. Kavelaars, F. Groenendaal, F. van Bel, and C. J. Heijnen, “Hypoxia/ischemia modulates G protein-coupled receptor kinase 2 and β-arrestin-1 levels in the neonatal rat brain,” Stroke 35(4), 981–986 (2004).
[Crossref] [PubMed]

2003 (2)

B. R. Vohr, W. C. Allan, M. Westerveld, K. C. Schneider, K. H. Katz, R. W. Makuch, and L. R. Ment, “School-age outcomes of very low birth weight infants in the indomethacin intraventricular hemorrhage prevention trial,” Pediatrics 111(4), e340–e346 (2003).
[Crossref] [PubMed]

H. J. Fullerton, Y. W. Wu, S. Zhao, and S. C. Johnston, “Risk of stroke in children: ethnic and gender disparities,” Neurology 61(2), 189–194 (2003).
[Crossref] [PubMed]

2001 (2)

S. Ruiz-Escusol, P. Medrano-Marina, M. Galván-Mansó, A. Marco-Tello, J. López-Pisón, and V. Rebage-Moisés, “Focal cerebral ischemic or hemorrhagic lesions in the term newborn. Review of the last decade,” Rev. Neurol. 32(9), 801–805 (2001).
[PubMed]

T. Anishchenko, N. Igosheva, T. Yakusheva, O. Glushkovskaya-Semyachkina, and O. Khokhlova, “Normalized entropy applied to the analysis of interindividual and gender-related differences in the cardiovascular effects of stress,” Eur. J. Appl. Physiol. 85(3-4), 287–298 (2001).
[Crossref] [PubMed]

1999 (3)

Y. Tomiyama, J. E. Brian, M. M. Todd, and W. Pearce, “Cerebral blood flow during hemodilution and hypoxia in rats : role of ATP-sensitive potassium channels,” Stroke 30(9), 1942–1948 (1999).
[Crossref] [PubMed]

D. Towner, M. A. Castro, E. Eby-Wilkens, and W. M. Gilbert, “Effect of mode of delivery in nulliparous women on neonatal intracranial injury,” N. Engl. J. Med. 341(23), 1709–1714 (1999).
[Crossref] [PubMed]

T. J. Benedetti, “Birth injury and method of delivery,” N. Engl. J. Med. 341(23), 1758–1759 (1999).
[Crossref] [PubMed]

1997 (3)

H. Ellekjaer, J. Holmen, B. Indredavik, and A. Terent, “Epidemiology of stroke in Innherred, Norway, 1994 to 1996. Incidence and 30-day case-fatality rate,” Stroke 28(11), 2180–2184 (1997).
[Crossref] [PubMed]

G. A. Taylor, “New concepts in the pathogenesis of germinal matrix intraparenchymal hemorrhage in premature infants,” AJNR Am. J. Neuroradiol. 18(2), 231–232 (1997).
[PubMed]

H. S. Ghazi-Birry, W. R. Brown, D. M. Moody, V. R. Challa, S. M. Block, and D. M. Reboussin, “Human germinal matrix: venous origin of hemorrhage and vascular characteristics,” AJNR Am. J. Neuroradiol. 18(2), 219–229 (1997).
[PubMed]

1995 (2)

G. A. Taylor, W. H. Trescher, M. V. Johnston, and R. J. Traysman, “Experimental neural injury in the newborn lamb: a comparison of NMDA receptor blockade and nitric oxide synthesis inhibition on lesion size and cerebral hyperemia,” Pediatr. Res. 38, 644–651 (1995).
[Crossref] [PubMed]

P. Bodin and G. Burnstock, “Synergistic effect of acute hypoxia on flow-induced release of ATP from cultured endothelial cells,” Experientia 51(3), 256–259 (1995).
[Crossref] [PubMed]

1991 (2)

J. F. Muzy, E. Bacry, and A. Arneodo, “Wavelets and multifractal formalism for singular signals: Application to turbulence data,” Phys. Rev. Lett. 67(25), 3515–3518 (1991).
[Crossref] [PubMed]

A. L. Goldberger, “Is the normal heartbeat chaotic or homeostatic?” News Physiol. Sci. 6, 87–91 (1991).
[PubMed]

1990 (1)

J. E. Skinner, A. L. Goldberger, G. Mayer-Kress, and R. E. Ideker, “Chaos in the heart: implication for clinical cardiology,” Nat. Biotechnol. 8(11), 1018–1024 (1990).
[Crossref]

1988 (1)

A. L. Goldberger, D. R. Rigney, J. Mietus, E. M. Antman, and S. Greenwald, “Nonlinear dynamics in sudden cardiac death syndrome: heartrate oscillations and bifurcations,” Experientia 44(11-12), 983–987 (1988).
[Crossref] [PubMed]

1987 (1)

F. Van Bel, M. Van de Bor, T. Stijnen, J. Baan, and J. H. Ruys, “Aetiological rôle of cerebral blood-flow alterations in development and extension of peri-intraventricular haemorrhage,” Dev. Med. Child Neurol. 29(5), 601–614 (1987).
[PubMed]

1986 (1)

A. Babloyantz and A. Destexhe, “Low-dimensional chaos in an instance of epilepsy,” Proc. Natl. Acad. Sci. U.S.A. 83(10), 3513–3517 (1986).
[Crossref] [PubMed]

1983 (1)

J. M. Perlman, J. B. McMenamin, and J. J. Volpe, “Fluctuating cerebral blood-flow velocity in respiratory-distress syndrome. Relation to the development of intraventricular hemorrhage,” N. Engl. J. Med. 309(4), 204–209 (1983).
[Crossref] [PubMed]

1982 (1)

R. J. Thorburn, A. P. Lipscomb, A. L. Stewart, E. O. R. Reynolds, and P. L. Hope, “Timing and antecedents of periventricular haemorrhage and of cerebral atrophy in very preterm infants,” Early Hum. Dev. 7(3), 221–238 (1982).
[Crossref] [PubMed]

1976 (1)

G. Hambleton and J. S. Wigglesworth, “Origin of intraventricular haemorrhage in the preterm infant,” Arch. Dis. Child. 51(9), 651–659 (1976).
[Crossref] [PubMed]

Ahn, S.

M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
[Crossref] [PubMed]

Akakin, A.

T. Kiliç and A. Akakin, “Anatomy of cerebral veins and sinuses,” Front Neurol. Neurosci. 23, 4–15 (2007).
[Crossref] [PubMed]

Al Hassani, L.

O. Semyachkina-Glushkovskaya, V. Lychagov, O. Bibikova, I. Semyachkin-Glushkovskiy, S. Sindeev, E. Zinchenko, M. Kassim, H. Braun, F. Al-Fatle, L. Al Hassani, and V. Tuchin, “The experimental study of stress-related pathological changes in cerebral venous blood flow in newborn rats assessed by DOCT,” J. Inn. Opt. Health Sci. 3(3), 1350023 (2013).

Alderliesten, T.

T. Alderliesten, P. M. Lemmers, J. J. Smarius, R. E. van de Vosse, W. Baerts, and F. van Bel, “Cerebral oxygenation, extraction, and autoregulation in very preterm infants who develop peri-intraventricular hemorrhage,” J. Pediatr. 162(4), 698–704 (2013).
[Crossref] [PubMed]

Al-Fatle, F.

O. Semyachkina-Glushkovskaya, V. Lychagov, O. Bibikova, I. Semyachkin-Glushkovskiy, S. Sindeev, E. Zinchenko, M. Kassim, H. Braun, F. Al-Fatle, L. Al Hassani, and V. Tuchin, “The experimental study of stress-related pathological changes in cerebral venous blood flow in newborn rats assessed by DOCT,” J. Inn. Opt. Health Sci. 3(3), 1350023 (2013).

Allan, W. C.

B. R. Vohr, W. C. Allan, M. Westerveld, K. C. Schneider, K. H. Katz, R. W. Makuch, and L. R. Ment, “School-age outcomes of very low birth weight infants in the indomethacin intraventricular hemorrhage prevention trial,” Pediatrics 111(4), e340–e346 (2003).
[Crossref] [PubMed]

Anishchenko, T.

T. Anishchenko, N. Igosheva, T. Yakusheva, O. Glushkovskaya-Semyachkina, and O. Khokhlova, “Normalized entropy applied to the analysis of interindividual and gender-related differences in the cardiovascular effects of stress,” Eur. J. Appl. Physiol. 85(3-4), 287–298 (2001).
[Crossref] [PubMed]

Antman, E. M.

A. L. Goldberger, D. R. Rigney, J. Mietus, E. M. Antman, and S. Greenwald, “Nonlinear dynamics in sudden cardiac death syndrome: heartrate oscillations and bifurcations,” Experientia 44(11-12), 983–987 (1988).
[Crossref] [PubMed]

Arneodo, A.

J. F. Muzy, E. Bacry, and A. Arneodo, “Wavelets and multifractal formalism for singular signals: Application to turbulence data,” Phys. Rev. Lett. 67(25), 3515–3518 (1991).
[Crossref] [PubMed]

Baan, J.

F. Van Bel, M. Van de Bor, T. Stijnen, J. Baan, and J. H. Ruys, “Aetiological rôle of cerebral blood-flow alterations in development and extension of peri-intraventricular haemorrhage,” Dev. Med. Child Neurol. 29(5), 601–614 (1987).
[PubMed]

Babloyantz, A.

A. Babloyantz and A. Destexhe, “Low-dimensional chaos in an instance of epilepsy,” Proc. Natl. Acad. Sci. U.S.A. 83(10), 3513–3517 (1986).
[Crossref] [PubMed]

Bacry, E.

J. F. Muzy, E. Bacry, and A. Arneodo, “Wavelets and multifractal formalism for singular signals: Application to turbulence data,” Phys. Rev. Lett. 67(25), 3515–3518 (1991).
[Crossref] [PubMed]

Baerts, W.

T. Alderliesten, P. M. Lemmers, J. J. Smarius, R. E. van de Vosse, W. Baerts, and F. van Bel, “Cerebral oxygenation, extraction, and autoregulation in very preterm infants who develop peri-intraventricular hemorrhage,” J. Pediatr. 162(4), 698–704 (2013).
[Crossref] [PubMed]

Ballabh, P.

P. Ballabh, “Intraventricular hemorrhage in premature infants: mechanism of disease,” Pediatr. Res. 67(1), 1–8 (2010).
[Crossref] [PubMed]

Basheer, S. N.

A. Michoulas, S. N. Basheer, E. H. Roland, K. Poskitt, S. Miller, and A. Hill, “The role of hypoxia-ischemia in term newborns with arterial stroke,” Pediatr. Neurol. 44(4), 254–258 (2011).
[Crossref] [PubMed]

Bassan, H.

H. Bassan, C. B. Benson, C. Limperopoulos, H. A. Feldman, S. A. Ringer, E. Veracruz, J. E. Stewart, J. S. Soul, D. N. Disalvo, J. J. Volpe, and A. J. du Plessis, “Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome,” Pediatrics 117(6), 2111–2118 (2006).
[Crossref] [PubMed]

Benedetti, T. J.

T. J. Benedetti, “Birth injury and method of delivery,” N. Engl. J. Med. 341(23), 1758–1759 (1999).
[Crossref] [PubMed]

Benson, C. B.

H. Bassan, C. B. Benson, C. Limperopoulos, H. A. Feldman, S. A. Ringer, E. Veracruz, J. E. Stewart, J. S. Soul, D. N. Disalvo, J. J. Volpe, and A. J. du Plessis, “Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome,” Pediatrics 117(6), 2111–2118 (2006).
[Crossref] [PubMed]

Beslow, L. A.

C. J. Bruno, L. A. Beslow, C. M. Witmer, A. Vossough, L. C. Jordan, S. Zelonis, D. J. Licht, R. N. Ichord, and S. E. Smith, “Haemorrhagic stroke in term and late preterm neonates,” Arch. Dis. Child. Fetal Neonatal Ed. 99(1), F48–F53 (2014).
[PubMed]

Bibikova, O.

O. Semyachkina-Glushkovskaya, V. Lychagov, O. Bibikova, I. Semyachkin-Glushkovskiy, S. Sindeev, E. Zinchenko, M. Kassim, H. Braun, F. Al-Fatle, L. Al Hassani, and V. Tuchin, “The experimental study of stress-related pathological changes in cerebral venous blood flow in newborn rats assessed by DOCT,” J. Inn. Opt. Health Sci. 3(3), 1350023 (2013).

A. Pavlov, O. Semyachkina-Glushkovskaya, O. Pavlova, O. Bibikova, and J. Kurths, “Wavelet-analysis of gastric microcirculation in rats with ulcer bleedings,” Eur. Phys. J. Spec. Top. 222(10), 2705–2712 (2013).
[Crossref]

Bibikova, O. A.

A. N. Pavlov, O. V. Semyachkina-Glushkovskaya, Y. Zhang, O. A. Bibikova, O. N. Pavlova, Q. Huang, D. Zhu, P. Li, V. V. Tuchin, and Q. Luo, “Multiresolution analysis of pathological changes in cerebral venous dynamics in newborn mice with intracranial hemorrhage: adrenorelated vasorelaxation,” Physiol. Meas. 35(10), 1983–1999 (2014).
[Crossref] [PubMed]

Block, S. M.

H. S. Ghazi-Birry, W. R. Brown, D. M. Moody, V. R. Challa, S. M. Block, and D. M. Reboussin, “Human germinal matrix: venous origin of hemorrhage and vascular characteristics,” AJNR Am. J. Neuroradiol. 18(2), 219–229 (1997).
[PubMed]

Bodin, P.

P. Bodin and G. Burnstock, “Synergistic effect of acute hypoxia on flow-induced release of ATP from cultured endothelial cells,” Experientia 51(3), 256–259 (1995).
[Crossref] [PubMed]

Braun, H.

O. Semyachkina-Glushkovskaya, V. Lychagov, O. Bibikova, I. Semyachkin-Glushkovskiy, S. Sindeev, E. Zinchenko, M. Kassim, H. Braun, F. Al-Fatle, L. Al Hassani, and V. Tuchin, “The experimental study of stress-related pathological changes in cerebral venous blood flow in newborn rats assessed by DOCT,” J. Inn. Opt. Health Sci. 3(3), 1350023 (2013).

Brian, J. E.

Y. Tomiyama, J. E. Brian, M. M. Todd, and W. Pearce, “Cerebral blood flow during hemodilution and hypoxia in rats : role of ATP-sensitive potassium channels,” Stroke 30(9), 1942–1948 (1999).
[Crossref] [PubMed]

Briers, D.

D. Briers, D. D. Duncan, E. Hirst, S. J. Kirkpatrick, M. Larsson, W. Steenbergen, T. Stromberg, and O. B. Thompson, “Laser speckle contrast imaging: theoretical and practical limitations,” J. Biomed. Opt. 18(6), 066018 (2013).
[Crossref] [PubMed]

Brouwer, A. J.

A. J. Brouwer, F. Groenendaal, C. Koopman, R. J. Nievelstein, S. K. Han, and L. S. de Vries, “Intracranial hemorrhage in full-term newborns: a hospital-based cohort study,” Neuroradiology 52(6), 567–576 (2010).
[Crossref] [PubMed]

Brown, W. R.

H. S. Ghazi-Birry, W. R. Brown, D. M. Moody, V. R. Challa, S. M. Block, and D. M. Reboussin, “Human germinal matrix: venous origin of hemorrhage and vascular characteristics,” AJNR Am. J. Neuroradiol. 18(2), 219–229 (1997).
[PubMed]

Bruno, C. J.

C. J. Bruno, L. A. Beslow, C. M. Witmer, A. Vossough, L. C. Jordan, S. Zelonis, D. J. Licht, R. N. Ichord, and S. E. Smith, “Haemorrhagic stroke in term and late preterm neonates,” Arch. Dis. Child. Fetal Neonatal Ed. 99(1), F48–F53 (2014).
[PubMed]

Bryant, D. M.

Burnstock, G.

P. Bodin and G. Burnstock, “Synergistic effect of acute hypoxia on flow-induced release of ATP from cultured endothelial cells,” Experientia 51(3), 256–259 (1995).
[Crossref] [PubMed]

Castro, M. A.

D. Towner, M. A. Castro, E. Eby-Wilkens, and W. M. Gilbert, “Effect of mode of delivery in nulliparous women on neonatal intracranial injury,” N. Engl. J. Med. 341(23), 1709–1714 (1999).
[Crossref] [PubMed]

Challa, V. R.

H. S. Ghazi-Birry, W. R. Brown, D. M. Moody, V. R. Challa, S. M. Block, and D. M. Reboussin, “Human germinal matrix: venous origin of hemorrhage and vascular characteristics,” AJNR Am. J. Neuroradiol. 18(2), 219–229 (1997).
[PubMed]

Chen, H.

A. Manaenko, H. Chen, J. H. Zhang, and J. Tang, “Comparison of different preclinical models of intracerebral hemorrhage,” Acta Neurochir. Suppl. (Wien) 111, 9–14 (2011).
[Crossref] [PubMed]

Chen, M. F.

S. C. Tang, H. I. Jen, Y. H. Lin, C. S. Hung, W. J. Jou, P. W. Huang, J. S. Shieh, Y. L. Ho, D. M. Lai, A. Y. Wu, J. S. Jeng, and M. F. Chen, “Complexity of heart rate variability predicts outcome in intensive care unit admitted patients with acute stroke,” J. Neurol. Neurosurg. Psychiatry 86(1), 95–100 (2015).
[Crossref] [PubMed]

Chescheir, N. C.

C. B. Looney, J. K. Smith, L. H. Merck, H. M. Wolfe, N. C. Chescheir, R. M. Hamer, and J. H. Gilmore, “Intracranial hemorrhage in asymptomatic neonates: prevalence on MR images and relationship to obstetric and neonatal risk factors,” Radiology 242(2), 535–541 (2007).
[Crossref] [PubMed]

Colbourne, F.

C. L. MacLellan, R. Paquette, and F. Colbourne, “A critical appraisal of experimental intracerebral hemorrhage research,” J. Cereb. Blood Flow Metab. 32(4), 612–627 (2012).
[Crossref] [PubMed]

Cousens, S.

J. E. Lawn, K. Kerber, C. Enweronu-Laryea, and S. Cousens, “3.6 million neonatal deaths - what is progressing and what is not?” Semin. Perinatol. 34(6), 371–386 (2010).
[Crossref] [PubMed]

Craft, T. K.

T. K. Craft, N. Zhang, E. R. Glasper, P. D. Hurn, and A. C. Devries, “Neonatal factors influence adult stroke outcome,” Psychoneuroendocrinology 31(5), 601–613 (2006).
[Crossref] [PubMed]

Cui, X.

Davies, N. P.

E. H. Whitby, P. D. Griffiths, S. Rutter, M. F. Smith, A. Sprigg, P. Ohadike, N. P. Davies, A. S. Rigby, and M. N. Paley, “Frequency and natural history of subdural haemorrhages in babies and relation to obstetric factors,” Lancet 363(9412), 846–851 (2004).
[Crossref] [PubMed]

Davis, M. A.

de Vries, L. S.

A. J. Brouwer, F. Groenendaal, C. Koopman, R. J. Nievelstein, S. K. Han, and L. S. de Vries, “Intracranial hemorrhage in full-term newborns: a hospital-based cohort study,” Neuroradiology 52(6), 567–576 (2010).
[Crossref] [PubMed]

Destexhe, A.

A. Babloyantz and A. Destexhe, “Low-dimensional chaos in an instance of epilepsy,” Proc. Natl. Acad. Sci. U.S.A. 83(10), 3513–3517 (1986).
[Crossref] [PubMed]

Deveber, G.

A. Kirton and G. Deveber, “Life after perinatal stroke,” Stroke 44(11), 3265–3271 (2013).
[Crossref] [PubMed]

Devries, A. C.

T. K. Craft, N. Zhang, E. R. Glasper, P. D. Hurn, and A. C. Devries, “Neonatal factors influence adult stroke outcome,” Psychoneuroendocrinology 31(5), 601–613 (2006).
[Crossref] [PubMed]

Disalvo, D. N.

H. Bassan, C. B. Benson, C. Limperopoulos, H. A. Feldman, S. A. Ringer, E. Veracruz, J. E. Stewart, J. S. Soul, D. N. Disalvo, J. J. Volpe, and A. J. du Plessis, “Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome,” Pediatrics 117(6), 2111–2118 (2006).
[Crossref] [PubMed]

Doepp, F.

J. M. Valdueza, F. Doepp, S. J. Schreiber, B. W. van Oosten, K. Schmierer, F. Paul, and M. P. Wattjes, “What went wrong? The flawed concept of cerebrospinal venous insufficiency,” J. Cereb. Blood Flow Metab. 33(5), 657–668 (2013).
[Crossref] [PubMed]

Du, C.

du Plessis, A. J.

H. Bassan, C. B. Benson, C. Limperopoulos, H. A. Feldman, S. A. Ringer, E. Veracruz, J. E. Stewart, J. S. Soul, D. N. Disalvo, J. J. Volpe, and A. J. du Plessis, “Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome,” Pediatrics 117(6), 2111–2118 (2006).
[Crossref] [PubMed]

Duckett, D. R.

M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
[Crossref] [PubMed]

Duncan, D. D.

D. Briers, D. D. Duncan, E. Hirst, S. J. Kirkpatrick, M. Larsson, W. Steenbergen, T. Stromberg, and O. B. Thompson, “Laser speckle contrast imaging: theoretical and practical limitations,” J. Biomed. Opt. 18(6), 066018 (2013).
[Crossref] [PubMed]

Dunn, A. K.

Eby-Wilkens, E.

D. Towner, M. A. Castro, E. Eby-Wilkens, and W. M. Gilbert, “Effect of mode of delivery in nulliparous women on neonatal intracranial injury,” N. Engl. J. Med. 341(23), 1709–1714 (1999).
[Crossref] [PubMed]

Ellekjaer, H.

H. Ellekjaer, J. Holmen, B. Indredavik, and A. Terent, “Epidemiology of stroke in Innherred, Norway, 1994 to 1996. Incidence and 30-day case-fatality rate,” Stroke 28(11), 2180–2184 (1997).
[Crossref] [PubMed]

Engel, M.

T. Takenouchi, E. Kasdorf, M. Engel, A. Grunebaum, and J. M. Perlman, “Changing pattern of perinatal brain injury in term infants in recent years,” Pediatr. Neurol. 46(2), 106–110 (2012).
[Crossref] [PubMed]

Enweronu-Laryea, C.

J. E. Lawn, K. Kerber, C. Enweronu-Laryea, and S. Cousens, “3.6 million neonatal deaths - what is progressing and what is not?” Semin. Perinatol. 34(6), 371–386 (2010).
[Crossref] [PubMed]

Fanaroff, A. A.

D. Wilson-Costello, H. Friedman, N. Minich, A. A. Fanaroff, and M. Hack, “Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s,” Pediatrics 115(4), 997–1003 (2005).
[Crossref] [PubMed]

Faraji, E.

Feldman, H. A.

H. Bassan, C. B. Benson, C. Limperopoulos, H. A. Feldman, S. A. Ringer, E. Veracruz, J. E. Stewart, J. S. Soul, D. N. Disalvo, J. J. Volpe, and A. J. du Plessis, “Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome,” Pediatrics 117(6), 2111–2118 (2006).
[Crossref] [PubMed]

Friedman, H.

D. Wilson-Costello, H. Friedman, N. Minich, A. A. Fanaroff, and M. Hack, “Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s,” Pediatrics 115(4), 997–1003 (2005).
[Crossref] [PubMed]

Fullerton, H. J.

H. J. Fullerton, Y. W. Wu, S. Zhao, and S. C. Johnston, “Risk of stroke in children: ethnic and gender disparities,” Neurology 61(2), 189–194 (2003).
[Crossref] [PubMed]

Galván-Mansó, M.

S. Ruiz-Escusol, P. Medrano-Marina, M. Galván-Mansó, A. Marco-Tello, J. López-Pisón, and V. Rebage-Moisés, “Focal cerebral ischemic or hemorrhagic lesions in the term newborn. Review of the last decade,” Rev. Neurol. 32(9), 801–805 (2001).
[PubMed]

Ghazi-Birry, H. S.

H. S. Ghazi-Birry, W. R. Brown, D. M. Moody, V. R. Challa, S. M. Block, and D. M. Reboussin, “Human germinal matrix: venous origin of hemorrhage and vascular characteristics,” AJNR Am. J. Neuroradiol. 18(2), 219–229 (1997).
[PubMed]

Gilbert, W. M.

D. Towner, M. A. Castro, E. Eby-Wilkens, and W. M. Gilbert, “Effect of mode of delivery in nulliparous women on neonatal intracranial injury,” N. Engl. J. Med. 341(23), 1709–1714 (1999).
[Crossref] [PubMed]

Gilmore, J. H.

C. B. Looney, J. K. Smith, L. H. Merck, H. M. Wolfe, N. C. Chescheir, R. M. Hamer, and J. H. Gilmore, “Intracranial hemorrhage in asymptomatic neonates: prevalence on MR images and relationship to obstetric and neonatal risk factors,” Radiology 242(2), 535–541 (2007).
[Crossref] [PubMed]

Glasper, E. R.

T. K. Craft, N. Zhang, E. R. Glasper, P. D. Hurn, and A. C. Devries, “Neonatal factors influence adult stroke outcome,” Psychoneuroendocrinology 31(5), 601–613 (2006).
[Crossref] [PubMed]

Glover, G. H.

Glushkovskaya-Semyachkina, O.

T. Anishchenko, N. Igosheva, T. Yakusheva, O. Glushkovskaya-Semyachkina, and O. Khokhlova, “Normalized entropy applied to the analysis of interindividual and gender-related differences in the cardiovascular effects of stress,” Eur. J. Appl. Physiol. 85(3-4), 287–298 (2001).
[Crossref] [PubMed]

Goldberger, A. L.

A. L. Goldberger, “Is the normal heartbeat chaotic or homeostatic?” News Physiol. Sci. 6, 87–91 (1991).
[PubMed]

J. E. Skinner, A. L. Goldberger, G. Mayer-Kress, and R. E. Ideker, “Chaos in the heart: implication for clinical cardiology,” Nat. Biotechnol. 8(11), 1018–1024 (1990).
[Crossref]

A. L. Goldberger, D. R. Rigney, J. Mietus, E. M. Antman, and S. Greenwald, “Nonlinear dynamics in sudden cardiac death syndrome: heartrate oscillations and bifurcations,” Experientia 44(11-12), 983–987 (1988).
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Y. Tomiyama, J. E. Brian, M. M. Todd, and W. Pearce, “Cerebral blood flow during hemodilution and hypoxia in rats : role of ATP-sensitive potassium channels,” Stroke 30(9), 1942–1948 (1999).
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Reynolds, E. O. R.

R. J. Thorburn, A. P. Lipscomb, A. L. Stewart, E. O. R. Reynolds, and P. L. Hope, “Timing and antecedents of periventricular haemorrhage and of cerebral atrophy in very preterm infants,” Early Hum. Dev. 7(3), 221–238 (1982).
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A. L. Goldberger, D. R. Rigney, J. Mietus, E. M. Antman, and S. Greenwald, “Nonlinear dynamics in sudden cardiac death syndrome: heartrate oscillations and bifurcations,” Experientia 44(11-12), 983–987 (1988).
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H. Bassan, C. B. Benson, C. Limperopoulos, H. A. Feldman, S. A. Ringer, E. Veracruz, J. E. Stewart, J. S. Soul, D. N. Disalvo, J. J. Volpe, and A. J. du Plessis, “Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome,” Pediatrics 117(6), 2111–2118 (2006).
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W. P. Riordan, P. R. Norris, J. M. Jenkins, and J. A. Morris., “Early loss of heart rate complexity predicts mortality regardless of mechanism, anatomic location, or severity of injury in 2178 trauma patients,” J. Surg. Res. 156(2), 283–289 (2009).
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A. Michoulas, S. N. Basheer, E. H. Roland, K. Poskitt, S. Miller, and A. Hill, “The role of hypoxia-ischemia in term newborns with arterial stroke,” Pediatr. Neurol. 44(4), 254–258 (2011).
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S. Ruiz-Escusol, P. Medrano-Marina, M. Galván-Mansó, A. Marco-Tello, J. López-Pisón, and V. Rebage-Moisés, “Focal cerebral ischemic or hemorrhagic lesions in the term newborn. Review of the last decade,” Rev. Neurol. 32(9), 801–805 (2001).
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E. H. Whitby, P. D. Griffiths, S. Rutter, M. F. Smith, A. Sprigg, P. Ohadike, N. P. Davies, A. S. Rigby, and M. N. Paley, “Frequency and natural history of subdural haemorrhages in babies and relation to obstetric factors,” Lancet 363(9412), 846–851 (2004).
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F. Van Bel, M. Van de Bor, T. Stijnen, J. Baan, and J. H. Ruys, “Aetiological rôle of cerebral blood-flow alterations in development and extension of peri-intraventricular haemorrhage,” Dev. Med. Child Neurol. 29(5), 601–614 (1987).
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J. M. Valdueza, F. Doepp, S. J. Schreiber, B. W. van Oosten, K. Schmierer, F. Paul, and M. P. Wattjes, “What went wrong? The flawed concept of cerebrospinal venous insufficiency,” J. Cereb. Blood Flow Metab. 33(5), 657–668 (2013).
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A. Pavlov, O. Semyachkina-Glushkovskaya, O. Pavlova, O. Bibikova, and J. Kurths, “Wavelet-analysis of gastric microcirculation in rats with ulcer bleedings,” Eur. Phys. J. Spec. Top. 222(10), 2705–2712 (2013).
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O. Semyachkina-Glushkovskaya, V. Lychagov, O. Bibikova, I. Semyachkin-Glushkovskiy, S. Sindeev, E. Zinchenko, M. Kassim, H. Braun, F. Al-Fatle, L. Al Hassani, and V. Tuchin, “The experimental study of stress-related pathological changes in cerebral venous blood flow in newborn rats assessed by DOCT,” J. Inn. Opt. Health Sci. 3(3), 1350023 (2013).

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A. N. Pavlov, O. V. Semyachkina-Glushkovskaya, Y. Zhang, O. A. Bibikova, O. N. Pavlova, Q. Huang, D. Zhu, P. Li, V. V. Tuchin, and Q. Luo, “Multiresolution analysis of pathological changes in cerebral venous dynamics in newborn mice with intracranial hemorrhage: adrenorelated vasorelaxation,” Physiol. Meas. 35(10), 1983–1999 (2014).
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M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
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E. H. Whitby, P. D. Griffiths, S. Rutter, M. F. Smith, A. Sprigg, P. Ohadike, N. P. Davies, A. S. Rigby, and M. N. Paley, “Frequency and natural history of subdural haemorrhages in babies and relation to obstetric factors,” Lancet 363(9412), 846–851 (2004).
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C. J. Bruno, L. A. Beslow, C. M. Witmer, A. Vossough, L. C. Jordan, S. Zelonis, D. J. Licht, R. N. Ichord, and S. E. Smith, “Haemorrhagic stroke in term and late preterm neonates,” Arch. Dis. Child. Fetal Neonatal Ed. 99(1), F48–F53 (2014).
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E. H. Whitby, P. D. Griffiths, S. Rutter, M. F. Smith, A. Sprigg, P. Ohadike, N. P. Davies, A. S. Rigby, and M. N. Paley, “Frequency and natural history of subdural haemorrhages in babies and relation to obstetric factors,” Lancet 363(9412), 846–851 (2004).
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D. Briers, D. D. Duncan, E. Hirst, S. J. Kirkpatrick, M. Larsson, W. Steenbergen, T. Stromberg, and O. B. Thompson, “Laser speckle contrast imaging: theoretical and practical limitations,” J. Biomed. Opt. 18(6), 066018 (2013).
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P. R. Norris, P. K. Stein, and J. A. Morris., “Reduced heart rate multiscale entropy predicts death in critical illness: a study of physiologic complexity in 285 trauma patients,” J. Crit. Care 23(3), 399–405 (2008).
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Stewart, A. L.

R. J. Thorburn, A. P. Lipscomb, A. L. Stewart, E. O. R. Reynolds, and P. L. Hope, “Timing and antecedents of periventricular haemorrhage and of cerebral atrophy in very preterm infants,” Early Hum. Dev. 7(3), 221–238 (1982).
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Stewart, J. E.

H. Bassan, C. B. Benson, C. Limperopoulos, H. A. Feldman, S. A. Ringer, E. Veracruz, J. E. Stewart, J. S. Soul, D. N. Disalvo, J. J. Volpe, and A. J. du Plessis, “Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome,” Pediatrics 117(6), 2111–2118 (2006).
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Stijnen, T.

F. Van Bel, M. Van de Bor, T. Stijnen, J. Baan, and J. H. Ruys, “Aetiological rôle of cerebral blood-flow alterations in development and extension of peri-intraventricular haemorrhage,” Dev. Med. Child Neurol. 29(5), 601–614 (1987).
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M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
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D. Briers, D. D. Duncan, E. Hirst, S. J. Kirkpatrick, M. Larsson, W. Steenbergen, T. Stromberg, and O. B. Thompson, “Laser speckle contrast imaging: theoretical and practical limitations,” J. Biomed. Opt. 18(6), 066018 (2013).
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Takenouchi, T.

T. Takenouchi, E. Kasdorf, M. Engel, A. Grunebaum, and J. M. Perlman, “Changing pattern of perinatal brain injury in term infants in recent years,” Pediatr. Neurol. 46(2), 106–110 (2012).
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D. Briers, D. D. Duncan, E. Hirst, S. J. Kirkpatrick, M. Larsson, W. Steenbergen, T. Stromberg, and O. B. Thompson, “Laser speckle contrast imaging: theoretical and practical limitations,” J. Biomed. Opt. 18(6), 066018 (2013).
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Thorburn, R. J.

R. J. Thorburn, A. P. Lipscomb, A. L. Stewart, E. O. R. Reynolds, and P. L. Hope, “Timing and antecedents of periventricular haemorrhage and of cerebral atrophy in very preterm infants,” Early Hum. Dev. 7(3), 221–238 (1982).
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Todd, M. M.

Y. Tomiyama, J. E. Brian, M. M. Todd, and W. Pearce, “Cerebral blood flow during hemodilution and hypoxia in rats : role of ATP-sensitive potassium channels,” Stroke 30(9), 1942–1948 (1999).
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Tomiyama, Y.

Y. Tomiyama, J. E. Brian, M. M. Todd, and W. Pearce, “Cerebral blood flow during hemodilution and hypoxia in rats : role of ATP-sensitive potassium channels,” Stroke 30(9), 1942–1948 (1999).
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Towers, A. J.

M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
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G. A. Taylor, W. H. Trescher, M. V. Johnston, and R. J. Traysman, “Experimental neural injury in the newborn lamb: a comparison of NMDA receptor blockade and nitric oxide synthesis inhibition on lesion size and cerebral hyperemia,” Pediatr. Res. 38, 644–651 (1995).
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Trescher, W. H.

G. A. Taylor, W. H. Trescher, M. V. Johnston, and R. J. Traysman, “Experimental neural injury in the newborn lamb: a comparison of NMDA receptor blockade and nitric oxide synthesis inhibition on lesion size and cerebral hyperemia,” Pediatr. Res. 38, 644–651 (1995).
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Tuchin, V.

O. Semyachkina-Glushkovskaya, V. Lychagov, O. Bibikova, I. Semyachkin-Glushkovskiy, S. Sindeev, E. Zinchenko, M. Kassim, H. Braun, F. Al-Fatle, L. Al Hassani, and V. Tuchin, “The experimental study of stress-related pathological changes in cerebral venous blood flow in newborn rats assessed by DOCT,” J. Inn. Opt. Health Sci. 3(3), 1350023 (2013).

Tuchin, V. V.

A. N. Pavlov, O. V. Semyachkina-Glushkovskaya, Y. Zhang, O. A. Bibikova, O. N. Pavlova, Q. Huang, D. Zhu, P. Li, V. V. Tuchin, and Q. Luo, “Multiresolution analysis of pathological changes in cerebral venous dynamics in newborn mice with intracranial hemorrhage: adrenorelated vasorelaxation,” Physiol. Meas. 35(10), 1983–1999 (2014).
[Crossref] [PubMed]

Valdueza, J. M.

J. M. Valdueza, F. Doepp, S. J. Schreiber, B. W. van Oosten, K. Schmierer, F. Paul, and M. P. Wattjes, “What went wrong? The flawed concept of cerebrospinal venous insufficiency,” J. Cereb. Blood Flow Metab. 33(5), 657–668 (2013).
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van Bel, F.

T. Alderliesten, P. M. Lemmers, J. J. Smarius, R. E. van de Vosse, W. Baerts, and F. van Bel, “Cerebral oxygenation, extraction, and autoregulation in very preterm infants who develop peri-intraventricular hemorrhage,” J. Pediatr. 162(4), 698–704 (2013).
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M. S. Lombardi, E. van den Tweel, A. Kavelaars, F. Groenendaal, F. van Bel, and C. J. Heijnen, “Hypoxia/ischemia modulates G protein-coupled receptor kinase 2 and β-arrestin-1 levels in the neonatal rat brain,” Stroke 35(4), 981–986 (2004).
[Crossref] [PubMed]

F. Van Bel, M. Van de Bor, T. Stijnen, J. Baan, and J. H. Ruys, “Aetiological rôle of cerebral blood-flow alterations in development and extension of peri-intraventricular haemorrhage,” Dev. Med. Child Neurol. 29(5), 601–614 (1987).
[PubMed]

Van de Bor, M.

F. Van Bel, M. Van de Bor, T. Stijnen, J. Baan, and J. H. Ruys, “Aetiological rôle of cerebral blood-flow alterations in development and extension of peri-intraventricular haemorrhage,” Dev. Med. Child Neurol. 29(5), 601–614 (1987).
[PubMed]

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T. Alderliesten, P. M. Lemmers, J. J. Smarius, R. E. van de Vosse, W. Baerts, and F. van Bel, “Cerebral oxygenation, extraction, and autoregulation in very preterm infants who develop peri-intraventricular hemorrhage,” J. Pediatr. 162(4), 698–704 (2013).
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M. S. Lombardi, E. van den Tweel, A. Kavelaars, F. Groenendaal, F. van Bel, and C. J. Heijnen, “Hypoxia/ischemia modulates G protein-coupled receptor kinase 2 and β-arrestin-1 levels in the neonatal rat brain,” Stroke 35(4), 981–986 (2004).
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J. M. Valdueza, F. Doepp, S. J. Schreiber, B. W. van Oosten, K. Schmierer, F. Paul, and M. P. Wattjes, “What went wrong? The flawed concept of cerebrospinal venous insufficiency,” J. Cereb. Blood Flow Metab. 33(5), 657–668 (2013).
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H. Bassan, C. B. Benson, C. Limperopoulos, H. A. Feldman, S. A. Ringer, E. Veracruz, J. E. Stewart, J. S. Soul, D. N. Disalvo, J. J. Volpe, and A. J. du Plessis, “Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome,” Pediatrics 117(6), 2111–2118 (2006).
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B. R. Vohr, W. C. Allan, M. Westerveld, K. C. Schneider, K. H. Katz, R. W. Makuch, and L. R. Ment, “School-age outcomes of very low birth weight infants in the indomethacin intraventricular hemorrhage prevention trial,” Pediatrics 111(4), e340–e346 (2003).
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Volpe, J. J.

H. Bassan, C. B. Benson, C. Limperopoulos, H. A. Feldman, S. A. Ringer, E. Veracruz, J. E. Stewart, J. S. Soul, D. N. Disalvo, J. J. Volpe, and A. J. du Plessis, “Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome,” Pediatrics 117(6), 2111–2118 (2006).
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J. M. Perlman, J. B. McMenamin, and J. J. Volpe, “Fluctuating cerebral blood-flow velocity in respiratory-distress syndrome. Relation to the development of intraventricular hemorrhage,” N. Engl. J. Med. 309(4), 204–209 (1983).
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C. J. Bruno, L. A. Beslow, C. M. Witmer, A. Vossough, L. C. Jordan, S. Zelonis, D. J. Licht, R. N. Ichord, and S. E. Smith, “Haemorrhagic stroke in term and late preterm neonates,” Arch. Dis. Child. Fetal Neonatal Ed. 99(1), F48–F53 (2014).
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J. M. Valdueza, F. Doepp, S. J. Schreiber, B. W. van Oosten, K. Schmierer, F. Paul, and M. P. Wattjes, “What went wrong? The flawed concept of cerebrospinal venous insufficiency,” J. Cereb. Blood Flow Metab. 33(5), 657–668 (2013).
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B. R. Vohr, W. C. Allan, M. Westerveld, K. C. Schneider, K. H. Katz, R. W. Makuch, and L. R. Ment, “School-age outcomes of very low birth weight infants in the indomethacin intraventricular hemorrhage prevention trial,” Pediatrics 111(4), e340–e346 (2003).
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M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
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E. H. Whitby, P. D. Griffiths, S. Rutter, M. F. Smith, A. Sprigg, P. Ohadike, N. P. Davies, A. S. Rigby, and M. N. Paley, “Frequency and natural history of subdural haemorrhages in babies and relation to obstetric factors,” Lancet 363(9412), 846–851 (2004).
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G. Hambleton and J. S. Wigglesworth, “Origin of intraventricular haemorrhage in the preterm infant,” Arch. Dis. Child. 51(9), 651–659 (1976).
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M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
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D. Wilson-Costello, H. Friedman, N. Minich, A. A. Fanaroff, and M. Hack, “Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s,” Pediatrics 115(4), 997–1003 (2005).
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C. J. Bruno, L. A. Beslow, C. M. Witmer, A. Vossough, L. C. Jordan, S. Zelonis, D. J. Licht, R. N. Ichord, and S. E. Smith, “Haemorrhagic stroke in term and late preterm neonates,” Arch. Dis. Child. Fetal Neonatal Ed. 99(1), F48–F53 (2014).
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C. B. Looney, J. K. Smith, L. H. Merck, H. M. Wolfe, N. C. Chescheir, R. M. Hamer, and J. H. Gilmore, “Intracranial hemorrhage in asymptomatic neonates: prevalence on MR images and relationship to obstetric and neonatal risk factors,” Radiology 242(2), 535–541 (2007).
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S. C. Tang, H. I. Jen, Y. H. Lin, C. S. Hung, W. J. Jou, P. W. Huang, J. S. Shieh, Y. L. Ho, D. M. Lai, A. Y. Wu, J. S. Jeng, and M. F. Chen, “Complexity of heart rate variability predicts outcome in intensive care unit admitted patients with acute stroke,” J. Neurol. Neurosurg. Psychiatry 86(1), 95–100 (2015).
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H. J. Fullerton, Y. W. Wu, S. Zhao, and S. C. Johnston, “Risk of stroke in children: ethnic and gender disparities,” Neurology 61(2), 189–194 (2003).
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M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
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Zelonis, S.

C. J. Bruno, L. A. Beslow, C. M. Witmer, A. Vossough, L. C. Jordan, S. Zelonis, D. J. Licht, R. N. Ichord, and S. E. Smith, “Haemorrhagic stroke in term and late preterm neonates,” Arch. Dis. Child. Fetal Neonatal Ed. 99(1), F48–F53 (2014).
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T. K. Craft, N. Zhang, E. R. Glasper, P. D. Hurn, and A. C. Devries, “Neonatal factors influence adult stroke outcome,” Psychoneuroendocrinology 31(5), 601–613 (2006).
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Zhang, Y.

A. N. Pavlov, O. V. Semyachkina-Glushkovskaya, Y. Zhang, O. A. Bibikova, O. N. Pavlova, Q. Huang, D. Zhu, P. Li, V. V. Tuchin, and Q. Luo, “Multiresolution analysis of pathological changes in cerebral venous dynamics in newborn mice with intracranial hemorrhage: adrenorelated vasorelaxation,” Physiol. Meas. 35(10), 1983–1999 (2014).
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Zhao, S.

H. J. Fullerton, Y. W. Wu, S. Zhao, and S. C. Johnston, “Risk of stroke in children: ethnic and gender disparities,” Neurology 61(2), 189–194 (2003).
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A. N. Pavlov, O. V. Semyachkina-Glushkovskaya, Y. Zhang, O. A. Bibikova, O. N. Pavlova, Q. Huang, D. Zhu, P. Li, V. V. Tuchin, and Q. Luo, “Multiresolution analysis of pathological changes in cerebral venous dynamics in newborn mice with intracranial hemorrhage: adrenorelated vasorelaxation,” Physiol. Meas. 35(10), 1983–1999 (2014).
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[Crossref] [PubMed]

Other (2)

J. Volpe, “Intracranial hemorrhage: Germinal matrix hemorrhage”, In: Neurology of the Newborn. 5th. Philadelphia, PA: Saunders Elsevier; 403–463 (2008)

Committee for the Update of the Guide for the Care and Use of Laboratory Animals, Institute for Laboratory Animal Research, Division on Earth and Life Studies, National Research Council of the National Academies, Guide for the care and use of laboratory animals. 8th edition. Washington: The National Academies Press; 2011. http://oacu.od.nih.gov/regs/guide/ guide.pdf . [Accessed 28 Feb 2012].

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Figures (4)

Fig. 1
Fig. 1

Cerebral vascular and parenchyma alterations induced by sound stress in newborn rats: a - the normal structure of vessels of the pia matter; b – congestion of excessive blood in the cerebral veins of the pia matter; c - perivascular edema; d - subcortical hemorrhage in low and high ( × 726.1) magnification; e - congestion of deep veins in the cerebral parenchyma; f - accumulation of blood in the microcirculatory vessels in the cortical and subcortical tissues. Hematoxylin & Eosin staining. Bars represent 10 µm ( × 246.4).

Fig. 2
Fig. 2

The relative cerebral blood flow assessed by LSCI in the sagittal sinus and in the small cerebral vessels (microcirculation) in newborn rats from the control, pre- and post-stroke groups.

Fig. 3
Fig. 3

Stress-related changes in the complexity measure Δ representing the width of the singularity spectrum D(h) of the venous CBF in newborn rats from the control, pre- and post-stroke groups.

Fig. 4
Fig. 4

The stress-related changes in beta-arrestin-1 levels in the brain.

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