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Transcranial ultrasonography as a reliable instrument for the measurement of the cerebral ventricles in rats with experimental hydrocephalus: a pilot study

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Abstract

Purposes

Demonstrate that transcranial ultrasonography (TUS) scanning is viable and useful as a diagnostic method in experimental hydrocephalus, as well as to compare measurements of cerebral and ventricular width obtained from TUS scans of hydrocephalic rats with post-mortem anatomical specimens, aiming for the development of accurate criteria to establish ventricular enlargement and progression of hydrocephalus subsequently.

Methods

Thirty-five male Wistar rats were used. Following hydrocephalus induction, they underwent a transcranial ultrasound scan to measure cerebral and ventricular dimensions, in the fourth and 21 post-induction days. By the end of the experiments, measurements obtained from TUS scans were compared with actual values as seen in the post-mortem specimens of each animal.

Results

Ventricular dilation could be clearly visualized in hydrocephalic animals. We performed intraclass correlation coefficient and linear regression analyses that have demonstrated a precise correlation between measurements of TUS scans and post-mortem specimens; we have found a similarity of 0,95 for the cerebral diameter and 0,97 for ventricular width.

Conclusions

Transcranial ultrasonography is a useful and reliable diagnostic tool for experimental hydrocephalus; also, it can be used to assess the progression of ventriculomegaly in animal models of hydrocephalus.

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References

  1. Rekate HL (2009) A contemporary definition and classification of hydrocephalus. Semin Pediatr Neurol 16:9–15

    Article  Google Scholar 

  2. Trevisi G, Frassanito P, Di Rocco C (2014) Idiopathic cerebrospinal fluid overproduction: case-based review of the pathophysiological mechanism implied in the cerebrospinal fluid production. Croat Med J 55:377–387

    Article  CAS  Google Scholar 

  3. Del Bigio MR, Di Curzio DL (2016) Nonsurgical therapy for hydrocephalus: a comprehensive and critical review. Fluids Barriers CNS 13:3

    Article  Google Scholar 

  4. Tully HM, Dobyns WB (2014) Infantile hydrocephalus: a review of epidemiology, classification, and causes. Eur J Med Genet 57:359–368

    Article  Google Scholar 

  5. Hanna RS, Essa AA, Makhlouf GA, Helmy AA (2019) Comparative study between laparoscopic and open techniques for insertion of ventriculoperitoneal shunt for treatment of congenital hydrocephalus. J Laparoendosc Adv Surg Tech A 29:109–113

    Article  Google Scholar 

  6. Langner S, Fleck S, Baldauf J, Mensel B, Kühn JP, Kirsch M (2017) Diagnosis and differential diagnosis of hydrocephalus in adults. Rofo 189:728–739

    Article  Google Scholar 

  7. Jain A, Swaminathan M (2015) Physics of ultrasound. Anaesth Pain & Intensive Care 19:533–539

    Google Scholar 

  8. Yulug B, Hanoglu L, Kilic E (2017) The neuroprotective effect of focused ultrasound: new perspectives on an old tool. Brain Res Bull 131:199–206

    Article  Google Scholar 

  9. Coatney RW (2001) Ultrasound imaging: principles and applications in rodent research. ILAR J 42:233–247

    Article  CAS  Google Scholar 

  10. Carvalho CF, Chammas M, Andrade Neto J, Jimenez C, Diniz S, Cerri G (2010) Transcranial duplex doppler in dogs with hydrocephalus. Arq Bras Med Vet Zootec 62:54–63

    Google Scholar 

  11. Miller DL (2008) Safety assurance in obstetrical ultrasound. Semin Ultrasound CT MR 29:156–164

    Article  Google Scholar 

  12. Li H, Sun J, Zhang D, Omire-Mayor D, Lewin PA, Tong S (2017) Low-intensity (400 mW/cm2, 500 kHz) pulsed transcranial ultrasound preconditioning may mitigate focal cerebral ischemia in rats. Brain Stimul 10:695–702

    Article  CAS  Google Scholar 

  13. Lopes LS, Slobodian I, Del Bigio MR (2009) Characterization of juvenile and young adult mice following induction of hydrocephalus with kaolin. Exp Neurol 219:187–196

    Article  CAS  Google Scholar 

  14. Silva SC, Feres O, da Silva BP, Machado HR, Menezes-Reis R, Araújo JE, Brandão RA, da Silva LL (2018) Hyperbaric oxygen therapy reduces astrogliosis and helps to recovery brain damage in hydrocephalic young rats. Childs Nerv Syst 34:1125–1134

    Article  Google Scholar 

  15. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Academic Press, San Diego, p 456

    Google Scholar 

  16. Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15:155–163

    Article  Google Scholar 

  17. Ludbrook J (2010) Linear regression analysis for comparing two measurers or methods of measurement: but which regression? Clin Exp Pharmacol Physiol 37:692–699

    Article  CAS  Google Scholar 

  18. Zacharias C, Alessio AM, Otto RK, Iyer RS, Philips GS, Swanson JO, Thapa MM (2013) Pediatric CT: strategies to lower radiation dose. AJR Am J Roentgenol 200:950–956

    Article  Google Scholar 

  19. Robson CD, MacDougall RD, Madsen JR, Warf BC, Robertson RL (2017) Neuroimaging of Children With Surgically Treated Hydrocephalus: A Practical Approach. AJR Am J Roentgenol 208:413–419

    Article  Google Scholar 

  20. Wolfson BJ, McAllister JP, Lovely TJ, Wright LC, Miller DW, Salotto AG (1989) Sonographic evaluation of experimental hydrocephalus in kittens. AJNR Am J Neuroradiol 10:1065–1067

    CAS  PubMed  Google Scholar 

  21. Brown JA, Rachlin J, Rubin JM, Wollmann RL (1984) Ultrasound evaluation of experimental hydrocephalus in dogs. Surg Neurol 22:273–276

    Article  CAS  Google Scholar 

  22. Catalão CHR, Shimizu GY, Tida JA, Garcia CAB, Dos Santos AC, Salmon CEG, Rocha MJA, da Silva LL (2017) Environmental enrichment reduces brain damage in hydrocephalic immature rats. Childs Nerv Syst 33:921–931

    Article  Google Scholar 

  23. Schmidt M, Ondreka N (2018) Hydrocephalus in Animals. Pediatr Hydroceph 1–53

  24. Stratmann G, Sall JW, May LD, Loepke AW, Lee MT (2010) Beyond anesthetic properties: the effects of isoflurane on brain cell death, neurogenesis, and long-term neurocognitive function. Anesth Analg 110:431–437

    Article  CAS  Google Scholar 

  25. Zhao P, Peng L, Li L, Xu X, Zuo Z (2007) Isoflurane preconditioning improves long-term neurologic outcome after hypoxic-ischemic brain injury in neonatal rats. Anesthesiology 107:963–970

    Article  CAS  Google Scholar 

  26. Li QF, Zhu YS, Jiang H (2008) Isoflurane preconditioning activates HIF-1alpha, iNOS, and Erk1/2 and protects against oxygen-glucose deprivation neuronal injury. Brain Res 1245:26–35

    Article  CAS  Google Scholar 

  27. Schifilliti D, Grasso G, Conti A, Fodale V (2010) Anaesthetic-related neuroprotection: intravenous or inhalational agents? CNS Drugs 24:893–907

    CAS  PubMed  Google Scholar 

  28. Tiran E, Ferrier J, Deffieux T, Gennisson JL, Pezet S, Lenkei Z, Tanter M (2017) Transcranial Functional Ultrasound Imaging in Freely Moving Awake Mice and Anesthetized Young Rats without Contrast Agent. Ultrasound Med Biol 43:1679–1689

    Article  Google Scholar 

  29. Gómez-de Frutos MC, García-Suárez I, Laso-García F, Diekhorst L, Otero-Ortega L, Alonso-López E, Díez-Tejedor E, Gutiérrez-Fernández M, Ruiz-Ares G (2020) Identification of brain structures and blood vessels by conventional ultrasound in rats. J Neurosci Methods 346:10893

    Article  Google Scholar 

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Acknowledgments

The authors are grateful to Antonio Renato Meirelles e Silva of the Laboratory of Applied and Experimental Neurology for his assistance with microscope photographs, Vanessa de Souza Nakagi of the Multiuser Ultrasound Laboratory, and Small Animal Echocardiography for performing transcranial ultrasound imaging tests and measurements.

Funding

Financial support from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP-2016/11212-7 and 2009/54010-1) and Fundação de Apoio ao Ensino, Pesquisa e Assistência do HCFMRP-USP (FAEPA-689/2018), gratefully acknowledged.

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Authors and Affiliations

  1. Ribeirão Preto College of Nursing, University of São Paulo, Bandeirantes Av., 3900, Ribeirão Preto, SP, 14049-900, Brazil

    Gabriel Aparecido Pinto de Moura Silva

  2. Department of Surgery and Anatomy, Ribeirão Preto Medical School, University of São Paulo, Bandeirantes Av., 3900, Ribeirão Preto, SP, 14049-900, Brazil

    Stephanya Covas da Silva, Pâmella da Silva Beggiora, Marcelo Volpon Santos, Hélio Rubens Machado & Luiza da Silva Lopes

  3. Laboratory of Neuroanatomy and Neuropsychobiology. Ribeirão Preto Medical School, University of São Paulo, Bandeirantes Av., 3900, Ribeirão Preto, SP, 14049-900, Brazil

    Ivair Matias Júnior

  4. Claretiano Centro Universitário, Dom Bôsco St., 466, Batatais, SP, 14300-000, Brazil

    Ivair Matias Júnior

  5. Institute of Health and Biotechnology, Federal University of Amazonas, Coari-Mamiá Road, 305, Coari, AM, 69460-000, Brazil

    Rafael Menezes-Reis

Authors
  1. Gabriel Aparecido Pinto de Moura Silva
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  2. Stephanya Covas da Silva
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  3. Pâmella da Silva Beggiora
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  4. Ivair Matias Júnior
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  5. Rafael Menezes-Reis
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  6. Marcelo Volpon Santos
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  7. Hélio Rubens Machado
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  8. Luiza da Silva Lopes
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Corresponding author

Correspondence to Stephanya Covas da Silva.

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Ethics approval

This study was designed according to the ethical guidelines published by the Brazilian College of Animal Experimentation (COBEA), protocol number 166/2015, and was approved by the Committee on Ethics in the Use of Animals of Ribeirão Preto Medical School, University of Sao Paulo (CEUA/FMRP-USP). All efforts have been made to minimize suffering and the number of animals used.

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The authors declare that they have no conflict of interest.

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de Moura Silva, G.A.P., da Silva, S.C., da Silva Beggiora, P. et al. Transcranial ultrasonography as a reliable instrument for the measurement of the cerebral ventricles in rats with experimental hydrocephalus: a pilot study. Childs Nerv Syst 37, 1863–1869 (2021). https://doi.org/10.1007/s00381-021-05070-6

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  • DOI: https://doi.org/10.1007/s00381-021-05070-6

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