Preview

Russian Pediatric Journal

Advanced search

Perinatal stroke: modelling and the potential of neurovisualization

https://doi.org/10.46563/1560-9561-2022-25-2-128-138

EDN: zxreyr

Abstract

Perinatal stroke (PS), characterized by sudden disappearance or impairment of brain functions, is a socially significant form of pathology that leads to the death and/or disability of children. Depending on the extent of the lesion, the severity of the consequences of a PS varies from a slight lag in learning to lifelong disability and inability to independently take care of yourself. The most common complications are cerebral palsy and epilepsy. Since the possibilities of diagnosis and therapy in the acute period are extremely limited, the efforts of health care providers and scientists are aimed at improving approaches to the rehabilitation of such patients. The authors presented an overview of modern methods of modelling PS in various experimental conditions. It is established that the modelling of PS is continuously being improved, new ways of forming ischemic brain damage are being created, each of which is necessary for the development of new scientific criteria for its early diagnosis and prediction of outcomes in standardized conditions. It is shown that a special place in the diagnosis of ischemic brain damage is occupied by wide-field optical visualization, which allows determining the formation of neural networks and functional maps of the cortex of the developing brain, provides an opportunity to analyze the spatiotemporal activity of neurons in large areas of the cerebral cortex and the processes of restoring cortical functions in the post-traumatic period. With the advent of genetically encoded ion sensor proteins and technologies for obtaining transgenic animal lines that specifically express sensors directly in neurons, opportunities have been created for optical registration of neural activity by analyzing changes in spontaneous activity of calcium signals and other mechanisms, which allows us to study brain neuroplasticity at a new level and create new ways to correct ischemic brain damage.

Contribution:
Surin A.M., Lizunova N.V., Kislukhina E.N. — concept and design;
Kislukhina E.N., Lizunova N.V. — collecting material, writing text;
Surin A.M. — editing.
Аll coauthors — аpproval of the final version of the article, responsibility for the integrity of all parts.

Acknowledgment. The study had no sponsorship.

Conflict of interest. The authors declare no conflict of interest.

Received: April 12, 2022
Accepted: April 26, 2022
Published: May 07, 2022

About the Authors

Natalia V. Lizunova
National Medical Research Center for Children’s Health; M.V. Lomonosov Moscow State University
Russian Federation

For correspondence: Natalia V. Lizunova, junior researcher at the Laboratory of neurobiology and fundamentals of brain development of the National Medical Research Center for Children’s Health, 119296 Moscow, Russian Federation; postgraduate student of the M.V. Lomonosov Moscow State University, Moscow, 119991, Russian Federation.

e-mail: natalia.lizunova18@mail.ru



Evgeniia N. Kislukhina
National Medical Research Center for Children’s Health
Russian Federation


Alexander M. Surin
National Medical Research Center for Children’s Health; Institute of General Pathology and Pathophysiology, Russian Academy of Medical Sciences
Russian Federation


References

1. Narogan M.V., Bychenko V.G., Ushakova L.V., Amirkhanova D.Yu., Ryumina I.I., Artamkina E.I., et al. Perinatal arterial ischemic stroke: incidence rate, diagnosis, clinical course variants, early outcomes. Pediatriya. Zhurnal im. G.N. Speranskogo. 2019; 98(2): 35–42. (in Russian). https://doi.org/10.24110/0031-403X-2019-98-2-35-42

2. Ferriero D.M., Fullerton H.J., Bernard T.J., Billinghurst L., Daniels S.R., Debaun M.R., et al. Management of stroke in neonates and children: a scientific statement from the American Heart Association/American Stroke Association. Stroke. 2019; 50(3): e51–96. https://doi.org/10.1161/STR.0000000000000183

3. Roach G.D. Perinatal arterial ischemic stroke. Neoreviews. 2020; 21(11): 741–8. https://doi.org/10.1542/neo.21-11-e741

4. Dunbar M., Kirton A. Perinatal stroke. Semin. Pediatr. Neurol. 2019; 32: 100767. https://doi.org/10.1016/J.SPEN.2019.08.003

5. Sorg A.L., Von Kries R., Klemme M., Gerstl L., Felderhoff-Müser U., Dzietko M. Incidence estimates of perinatal arterial ischemic stroke in preterm- and term-born infants: a National Capture-Recapture Calculation Corrected Surveillance Study. Neonatology. 2021; 118(6): 727–33. https://doi.org/10.1159/000514922

6. Li C., Miao J.K., Xu Y., Hua Y.Y., Ma Q., Zhou L.L., et al. Prenatal, perinatal and neonatal risk factors for perinatal arterial ischaemic stroke: a systematic review and meta-analysis. Eur. J. Neurol. 2017; 24(8): 1006–15. https://doi.org/10.1111/ENE.13337

7. Lin B., Zhang Z., Mei Y., Wang C., Xu H., Liu L., et al. Cumulative risk of stroke recurrence over the last 10 years: a systematic review and meta-analysis. Neurol. Sci. 2021; 42(1): 61–71. https://doi.org/10.1007/s10072-020-04797-5/tables/4

8. Roy B., Arbuckle S., Walker K., Morgan C., Galea C., Badawi N., et al. The role of the placenta in perinatal stroke: a systematic review. J. Child Neurol. 2020; 35(11): 773–83. https://doi.org/10.1177/0883073820929214

9. Rattani A., Lim J., Mistry A.M., Prablek M.A., Roth S.G., Jordan L.C., et al. Incidence of epilepsy and associated risk factors in perinatal ischemic stroke survivors. Pediatr. Neurol. 2019; 90: 44–55. https://doi.org/10.1016/j.pediatrneurol.2018.08.025

10. Kirton A., Metzler M.J., Craig B.T., Hilderley A., Dunbar M., Giuffre A., et al. Perinatal stroke: mapping and modulating developmental plasticity. Nat. Rev. Neurol. 2021; 17(7): 415–32. https://doi.org/10.1038/s41582-021-00503-x

11. Baker K., Carlson H.L., Zewdie E., Kirton A. Developmental remodelling of the motor cortex in hemiparetic children with perinatal stroke. Pediatr. Neurol. 2020; 112: 34–43. https://doi.org/10.1016/j.pediatrneurol.2020.08.004

12. Kuczynski A.M., Semrau J.A., Kirton A., Dukelow S.P. Kinesthetic deficits after perinatal stroke: robotic measurement in hemiparetic children. J. Neuroeng. Rehabil. 2017; 14(1): 13. https://doi.org/10.1186/S12984-017-0221-6

13. Koenraads Y., Porro G.L., Braun K.P.J., Groenendaal F., De Vries L.S., Van Der Aa N.E. Prediction of visual field defects in newborn infants with perinatal arterial ischemic stroke using early MRI and DTI-based tractography of the optic radiation. Eur. J. Paediatr. Neurol. 2016; 20(2): 309–18. https://doi.org/10.1016/j.ejpn.2015.11.010

14. Lidzba K., de Haan B., Wilke M., Krägeloh-Mann I., Staudt M. Lesion characteristics driving right-hemispheric language reorganization in congenital left-hemispheric brain damage. Brain Lang. 2017; 173: 1–9. https://doi.org/10.1016/J.BANDL.2017.04.006

15. Hamada S., Ogawa I., Yamasaki M., Kiyama Y., Kassai H., Watabe A.M., et al. The glutamate receptor GluN2 subunit regulates synaptic trafficking of AMPA receptors in the neonatal mouse brain. Eur. J. Neurosci. 2014; 40(8): 3136–46. https://doi.org/10.1111/EJN.12682

16. Perrone S., Laschi E., Buonocore G. Oxidative stress biomarkers in the perinatal period: Diagnostic and prognostic value. Semin. Fetal Neonatal Med. 2020; 25(2): 101087. https://doi.org/10.1016/j.siny.2020.101087

17. Spaas J., van Veggel L., Schepers M., Tiane A., van Horssen J., Wilson D.M., et al. Oxidative stress and impaired oligodendrocyte precursor cell differentiation in neurological disorders. Cell. Mol. Life Sci. 2021; 78(10): 4615–37. https://doi.org/10.1007/S00018-021-03802-0

18. Ohtaka-Maruyama C. Subplate neurons as an organizer of mammalian neocortical development. Front. Neuroanat. 2020; 14: 8. https://doi.org/10.3389/fnana.2020.00008

19. Hu B.R., Liu C.L., Ouyang Y., Blomgren K., Siesjö B.K. Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation. J. Cereb. Blood Flow Metab. 2000; 20(9): 1294–300. https://doi.org/10.1097/00004647-200009000-00003

20. Mineyko A., Nettel-Aguirre A., de Jesus P., Benseler S., Yusuf K., Narendran A., et al. Association of neonatal inflammatory markers and perinatal stroke subtypes. Neurology. 2020; 95(9): e1163–73. https://doi.org/10.1212/WNL.0000000000010309

21. Fernández-López D., Faustino J., Klibanov A.L., Derugin N., Blanchard E., Simon F., et al. Microglial cells prevent hemorrhage in neonatal focal arterial stroke. J. Neurosci. 2016; 36(10): 2881–93. https://doi.org/10.1523/jneurosci.0140-15.2016

22. Fernández-López D., Faustino J., Daneman R., Zhou L., Lee S.Y., Derugin N., et al. Blood–brain barrier permeability is increased after acute adult stroke but not neonatal stroke in the rat. J. Neurosci. 2012; 32(28): 9588. https://doi.org/10.1523/JNEUROSCI.5977-11.2012

23. Langen U.H., Ayloo S., Gu C. Development and cell biology of the blood-brain barrier. Annu. Rev. Cell Dev. Biol. 2019; 35: 591–613. https://doi.org/10.1146/annurev-cellbio-100617-062608

24. Fajardo-Fregoso B.F., Castañeda-Cabral J.L., Beas-Zárate C., Ureña-Guerrero M.E. Neonatal excitotoxicity modifies blood-brain barrier properties increasing its susceptibility to hypertonic shock in adulthood. Int. J. Dev. Neurosci. 2020; 80(4): 335–46. https://doi.org/10.1002/JDN.10027

25. Yang Z., Covey M.V., Bitel C.L., Ni L., Jonakait G.M., Levison S.W. Sustained neocortical neurogenesis after neonatal hypoxic/ischemic injury. Ann. Neurol. 2007; 61(3): 199–208. https://doi.org/10.1002/ana.21068

26. Fernández-López D., Faustino J., Derugin N., Vexler Z.S. Acute and chronic vascular responses to experimental focal arterial stroke in the neonate rat. Transl. Stroke Res. 2013; 4(2): 179. https://doi.org/10.1007/S12975-012-0214-5

27. Zhang S.Y., Jeffers M.S., Lagace D.C., Kirton A., Silasi G. Developmental and interventional plasticity of motor maps after perinatal stroke. J. Neurosci. 2021; 41(28): 6157–72. https://doi.org/10.1523/JNEUROSCI.3185-20.2021

28. Zewdie E., Damji O., Ciechanski P., Seeger T., Kirton A. Contralesional corticomotor neurophysiology in hemiparetic children with perinatal stroke: developmental plasticity and clinical function. Neurorehabil. Neural Repair. 2017; 31(3): 261–71. https://doi.org/10.1177/1545968316680485

29. Craig B.T., Olsen C., Mah S., Carlson H.L., Wei X.C., Kirton A. Crossed cerebellar atrophy in perinatal stroke. Stroke. 2019; 50(1): 175–7. https://doi.org/10.1161/strokeaha.118.022423

30. Craig B.T., Carlson H.L., Kirton A. Thalamic diaschisis following perinatal stroke is associated with clinical disability. Neuroimage Clin. 2019; 21: 101660. https://doi.org/10.1016/J.NICL.2019.101660

31. Titomanlio L., Fernández-López D., Manganozzi L., Moretti R., Vexler Z.S., Gressens P. Pathophysiology and neuroprotection of global and focal perinatal brain injury: lessons from animal models. Pediatr. Neurol. 2015; 52(6): 566–84. https://doi.org/10.1016/j.pediatrneurol.2015.01.016

32. Sporns P.B., Fullerton H.J., Lee S., Kirton A., Wildgruber M. Current treatment for childhood arterial ischaemic stroke. Lancet Child Adolesc. Heal. 2021; 5(11): 825–36. https://doi.org/10.1016/S2352-4642(21)00167-X

33. Vandamme T.F. Rodent models for human diseases. Eur. J. Pharmacol. 2015; 759: 84–9. https://doi.org/10.1016/j.ejphar.2015.03.046

34. Eyre J.A. Corticospinal tract development and its plasticity after perinatal injury. Neurosci. Biobehav. Rev. 2007; 31(8): 1136–49. https://doi.org/10.1016/j.neubiorev.2007.05.011

35. Mitsuie T., Nakamura S., Htun Y., Nakao Y., Arioka M., Koyano K., et al. Cerebral blood volume increment after resuscitation measured by near-infrared time-resolved spectroscopy can estimate degree of hypoxic–ischemic insult in newborn piglets. Sci. Rep. 2021; 11(1): 1–10. https://doi.org/10.1038/s41598-021-92586-1

36. Robertson N.J., Meehan C., Martinello K.A., Avdic-Belltheus A., Boggini T., Mutshiya T., et al. Human umbilical cord mesenchymal stromal cells as an adjunct therapy with therapeutic hypothermia in a piglet model of perinatal asphyxia. Cytotherapy. 2021; 23(6): 521–35. https://doi.org/10.1016/j.jcyt.2020.10.005

37. Rice J.E., Vannucci R.C., Brierley J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 1981; 9(2): 131–41. https://doi.org/10.1002/ana.410090206

38. Hamdy N., Eide S., Sun H.S., Feng Z.P. Animal models for neonatal brain injury induced by hypoxic ischemic conditions in rodents. Exp. Neurol. 2020; 334: 113457. https://doi.org/10.1016/j.expneurol.2020.113457

39. Vannucci R.C., Vannucci S.J. A model of perinatal hypoxic-ischemic brain damage. Ann. N.Y. Acad. Sci. 1997; 835: 234–49. https://doi.org/10.1111/J.1749-6632.1997.TB48634.X

40. Alexander M., Garbus H., Smith A.L., Rosenkrantz T.S., Fitch R.H. Behavioral and histological outcomes following neonatal HI injury in a preterm (P3) and term (P7) rodent model. Behav. Brain Res. 2014; 259: 85–96. https://doi.org/10.1016/J.BBR.2013.10.038

41. Ek C.J., D’angelo B., Baburamani A.A., Lehner C., Leverin A.L., Smith P.L.P., et al. Brain barrier properties and cerebral blood flow in neonatal mice exposed to cerebral hypoxia-ischemia. J. Cereb. Blood Flow Metab. 2015; 35(5): 818–27. https://doi.org/10.1038/jcbfm.2014.255

42. Edwards A.B., Feindel K.W., Cross J.L., Anderton R.S., Clark V.W., Knuckey N.W., et al. Modification to the Rice-Vannucci perinatal hypoxic-ischaemic encephalopathy model in the P7 rat improves the reliability of cerebral infarct development after 48 hours. J. Neurosci. Methods. 2017; 288: 62–71. https://doi.org/10.1016/j.jneumeth.2017.06.016

43. Ashwal S., Cole D.J., Osborne S., Osborne T.N., Pearce W.J. A new model of neonatal stroke: Reversible middle cerebral artery occlusion in the rat pup. Pediatr. Neurol. 1995; 12(3): 191–6. https://doi.org/10.1016/0887-8994(95)00006-2

44. Larpthaveesarp A., Gonzalez F.F. Transient middle cerebral artery occlusion model of neonatal stroke in P10 rats. J. Vis. Exp. 2017; 2017(122): e54830. https://doi.org/10.3791/54830

45. Derugin N., Ferriero D.M., Vexler Z.S. Neonatal reversible focal cerebral ischemia: a new model. Neurosci. Res. 1998; 32(4): 349–53. https://doi.org/10.1016/S0168-0102(98)00096-0

46. Brima T., Mikulecká A., Otáhal J. Impacts of perinatal induced photothrombotic stroke on sensorimotor performance in adult rats. Physiol. Res. 2013; 62(1): 85–94. https://doi.org/10.33549/physiolres.932447

47. Chumak T., Lecuyer M.J., Nilsson A.K., Faustino J., Ardalan M., Svedin P., et al. Maternal n-3 polyunsaturated fatty acid enriched diet commands fatty acid composition in postnatal brain and protects from neonatal arterial focal stroke. Transl. Stroke Res. 2021; 13, 449–46. https://doi.org/10.1007/s12975-021-00947-9

48. Renolleau S., Aggoun-Zouaoui D., Ben-Ari Y., Charriaut-Marlangue C.A. Model of transient unilateral focal ischemia with reperfusion in the P7 neonatal rat. Stroke. 1998; 29(7): 1454–61. https://doi.org/10.1161/01.STR.29.7.1454

49. Tsuji M., Ohshima M., Taguchi A., Kasahara Y., Ikeda T., Matsuyama T. A novel reproducible model of neonatal stroke in mice: Comparison with a hypoxia–ischemia model. Exp. Neurol. 2013; 247: 218–25. https://doi.org/10.1016/j.expneurol.2013.04.015

50. Tanaka E., Ogawa Y., Mukai T., Sato Y., Hamazaki T., Nagamura-Inoue T., et al. Dose-dependent effect of intravenous administration of human umbilical cord-derived mesenchymal stem cells in neonatal stroke mice. Front. Neurol. 2018; 9: 133. https://doi.org/10.3389/fneur.2018.00133

51. Faustino J.V., Wang X., Johnson C.E., Klibanov A., Derugin N., Wendland M.F., et al. Neurobiology of disease microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke. J. Neurosci.. 2011; 31(36): 12992–3001. https://doi.org/10.1523/jneurosci.2102-11.2011

52. Ceprián M., Jiménez-Sánchez L., Vargas C., Barata L., Hind W., Martínez-Orgado J. Cannabidiol reduces brain damage and improves functional recovery in a neonatal rat model of arterial ischemic stroke. Neuropharmacology. 2017; 116: 151–9. https://doi.org/10.1016/j.neuropharm.2016.12.017

53. Jia J.M., Peng C., Wang Y., Zheng J., Ge W.P. Control of occlusion of middle cerebral artery in perinatal and neonatal mice with magnetic force. Mol. Brain. 2018; 11(1): 47. https://doi.org/10.1186/S13041-018-0389-0/figures/6

54. Watson B.D., Dietrich W.D., Busto R., Wachtel M.S., Ginsberg M.D. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann. Neurol. 1985; 17(5): 497–504. https://doi.org/10.1002/ana.410170513

55. Maxwell K.A., Dyck R.H. Induction of reproducible focal ischemic lesions in neonatal mice by photothrombosis. Dev. Neurosci. 2005; 27(2–4): 121–6. https://doi.org/10.1159/000085983

56. Tuor U.I., Qiao M., Sule M., Morgunov M., Foniok T. Magnetic resonance imaging of ischemic injury produced by varying severities of photothrombosis differs in neonatal and adult brain. NMR Biomed. 2016; 29(12): 1700–8. https://doi.org/10.1002/nbm.3626

57. Nakayama H., Dalton D.W., Watson B.D., Busto R., Ginsberg M.D. Journal of cerebral blood flow and metabolism photo thrombotic occlusion of rat middle cerebral artery: histopathological and hemodynamic sequelae of acute recanalization. J. Cereb. Blood Flow Metab. 1988; 8(3): 357–66. https://doi.org/10.1038/jcbfm.1988.71

58. Watson B.D., Prado R., Veloso A., Brunschwig J.P., Dietrich W.D. Cerebral blood flow restoration and reperfusion injury after ultraviolet laser–facilitated middle cerebral artery recanalization in rat thrombotic stroke. Stroke. 2002; 33(2): 428–34. https://doi.org/10.1161/hs0202.102730

59. Yi Y.Y., Shin H.J., Choi S.G., Kang J.W., Song H.J., Kim S.K., et al. Preventive effects of neuroprotective agents in a neonatal rat of photothrombotic stroke model. Int. J. Mol. Sci. 2020; 21(10): 3703. https://doi.org/10.3390/ijms21103703

60. Gennaro M., Mattiello A., Pizzorusso T. Rodent models of developmental ischemic stroke for translational research: Strengths and weaknesses. Neural. Plast. 2019; 2019: 5089321. https://doi.org/10.1155/2019/5089321

61. Hillman E.M.C. Coupling mechanism and significance of the BOLD Signal: A status report. Annu. Rev. Neurosci. 2014; 37: 161–81. https://doi.org/10.1146/annurev-neuro-071013-014111

62. Hillman E.M.C. Optical brain imaging in vivo: techniques and applications from animal to man. J. Biomed. Opt. 2007; 12(5): 051402. https://doi.org/10.1117/1.2789693

63. White B.R., Padawer-Curry J.A., Cohen A.S., Licht D.J., Yodh A.G. Brain segmentation, spatial censoring, and averaging techniques for optical functional connectivity imaging in mice. Biomed. Opt. Express. 2019; 10(11): 5952–73. https://doi.org/10.1364/boe.10.005952

64. Ma Y., Shaik M.A., Kim S.H., Kozberg M.G., Thibodeaux D.N., Zhao H.T., et al. Wide-field optical mapping of neural activity and brain haemodynamics: considerations and novel approaches. Philos. Trans. R. Soc. B Biol. Sci. 2016; 371(1705): 20150360. https://doi.org/10.1098/rstb.2015.0360

65. Tian L., Hires S.A., Mao T., Huber D., Chiappe M.E., Chalasani S.H., et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods. 2009; 6(12): 875–81. https://doi.org/10.1038/nmeth.1398

66. West S.L., Aronson J.D., Popa L.S., Feller K.D., Carter R.E., Chiesl W.M., et al. Wide-field calcium imaging of dynamic cortical networks during locomotion. Cereb Cortex. 2021; bhab373. https://doi.org/10.1093/cercor/bhab373

67. Cross C.M., Santos L.M., Whiteley N., Luyt K., Ashby M.C. Early functional connectivity in the developing sensorimotor network that is independent of sensory experience. bioRxiv. 2021; 2021.06.14.448057. https://doi.org/10.1101/2021.06.14.448057

68. Kozberg M.G., Ma Y., Shaik M.A., Kim S.H., Hillman E.M.C. Rapid postnatal expansion of neural networks occurs in an environment of altered neurovascular and neurometabolic coupling. J. Neurosci. 2016; 36(25): 6704–17. https://doi.org/10.1523/jneurosci.2363-15.2016

69. Murphy T.H., Corbett D. Plasticity during stroke recovery: from synapse to behaviour. Nat. Rev. Neurosci. 2009; 10(12): 861–72. https://doi.org/10.1038/nrn2735

70. Winship I.R., Murphy T.H. In vivo calcium imaging reveals functional rewiring of single somatosensory neurons after stroke. J. Neurosci. 2008; 28(26): 6592–606. https://doi.org/10.1523/jneurosci.0622-08.200


Review

For citations:


Lizunova N.V., Kislukhina E.N., Surin A.M. Perinatal stroke: modelling and the potential of neurovisualization. Russian Pediatric Journal. 2022;25(2):128-138. (In Russ.) https://doi.org/10.46563/1560-9561-2022-25-2-128-138. EDN: zxreyr

Views: 137


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 1560-9561 (Print)
ISSN 2413-2918 (Online)