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A New Model of Experimental Hemispherotomy in Young Adult Rattus Norvegicus: a Neural Tract Tracing and SPECT in Vivo Study

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A New Model of Experimental Hemispherotomy in Young Adult Rattus Norvegicus: a Neural Tract Tracing and SPECT in Vivo Study LABORATORY INVESTIGATION A new model of experimental hemispherotomy in young adult Rattus norvegicus: a neural tract tracing and SPECT in vivo study Ivair Matias Jr., ScM,1,2 Daoud Hibrahim Elias-Filho,2 Camila Araújo Bernardino Garcia, ScM,1 Guilherme Henrique Silva,1 Jorge Mejia, ScD,3 Francisco Romero Cabral, ScD,3 Ana Cláudia Camargo Miranda, ScM,3 Sérgio Gomes da Silva, ScD,3,5 Luíza da Silva Lopes, MD, ScD,1 Norberto Cysne Coimbra, MD, ScM, ScD,2,4 and Hélio Rubens Machado, MD, ScM, ScD1,4 1Laboratory of Pediatric Neurosurgery and Developmental Neuropathology, Department of Surgery and Anatomy, 2Laboratory of Neuroanatomy and Neuropsychobiology, Department of Pharmacology, and 4Neuroelectrophysiology Multiuser Centre and Neurobiology of Pain and Emotions Laboratory, Department of Surgery and Anatomy, Ribeirão Preto Medical School of the University of São Paulo; 3Hospital Israelita Albert Einstein; and 5Núcleo de Pesquisas Tecnológicas (NPT), Universidade de Mogi das Cruzes, São Paulo, Brazil OBJECTIVE The objective of this study was to describe a new experimental model of hemispherotomy performed on laboratory animals. METHODS Twenty-six male young adult Wistar rats were distributed into two groups (surgery and control). The nonfluo- rescent anterograde neurotracer biotinylated dextran amine (BDA; 10,000 MW) was microinjected into the motor cortex area (M1) according to The Rat Brain in Stereotaxic Coordinates atlas to identify pathways and fibers disconnected after the experimental hemispherectomy. SPECT tomographic images of 99mTc hexamethylpropyleneamine oxime were ob- tained to verify perfusion in functioning areas of the disconnected and intact brain. A reproducible and validated surgical procedure is described in detail, including exact measurements and anatomical relationships. An additional 30 rodents (n = 10 rats per group) were divided into naïve, sham, and hemispherotomy groups and underwent the rotarod test. RESULTS Cortico-cortical neural pathways were identified crossing the midline and contacting neuronal perikarya in the contralateral brain hemisphere in controls, but not in animals undergoing hemispherotomy. There was an absence of perfusion in the left side of the brain of the animals undergoing hemispherotomy. Motor performance was significantly af- fected by brain injuries, increasing the number of attempts to maintain balance on the moving cylinder in the rotarod test at 10 and 30 days after the hemispherotomy, with a tendency to minimize the motor performance deficit over time. CONCLUSIONS The present findings show that the technique reproduced neural disconnection with minimal resection of brain parenchyma in young adult rats, thereby duplicating the hemispherotomy procedures in human patients. https://thejns.org/doi/abs/10.3171/2017.12.JNS171150 KEYWORDS hemispherotomy; biotinylated dextran amine neurotracer; cerebral cortex; corpus callosum; small-animal SPECT; epilepsy EMISPHERECTOMY has been used for decades in the scribed as an effective surgical technique for hemispheric treatment of children with refractory epilepsy and disconnection.14,48 This technique allows a complete dis- unilateral hemispheric lesions. While anatomi- connection between both brain hemispheres with good Hcal hemispherectomy is still performed, other techniques, results regarding seizure control; it also causes minimal such as hemispherotomy and functional hemispherectomy, intraoperative bleeding and the shortest possible surgical are now also used to disconnect a cerebral hemisphere.37,48 time, with small skin incisions, craniotomies, and the least Introduced in the 1990s, hemispherotomy has been de- possible resection of the cerebral parenchyma.13 A system- ABBREVIATIONS BDA = biotinylated dextran amine; CPu = caudatus/putamen; HMPAO = hexamethylpropyleneamine oxime. SUBMITTED May 9, 2017. ACCEPTED December 11, 2017. INCLUDE WHEN CITING Published online June 8, 2018; DOI: 10.3171/2017.12.JNS171150. ©AANS 2018, except where prohibited by US copyright law J Neurosurg June 8, 2018 1 Unauthenticated | Downloaded 10/03/21 10:42 PM UTC I. Matias Jr. et al. atic review of the literature related to hemispherotomy for of the Ribeirão Preto Medical School of the University of the treatment of refractory epilepsy found that this surgical São Paulo and of the Hospital Israelita Albert Einstein in procedure is highly effective in the treatment of refractory agreement with the animal research ethics adopted by the epilepsy in children, particularly considering acquired National Council for Animal Experimentation Control, and progressive etiologies, and that hemispherotomy pro- affiliated with the International Council for Laboratory cedures are associated with a more favorable complication Animal Science. All efforts were made to minimize suf- profile.36 fering, as well as the number of animals used in this study. The clinical examination after functional hemispherec- tomy in children often demonstrates the presence of func- Experimental Groups tional deficits in the proximal and distal muscles of the Rats were distributed into two experimental groups for contralateral side to the surgical intervention. The hand neural tract tracing and SPECT procedures (n = 26). Neu- and wrist functions have the highest deficits (94%), fol- ral tract tracing (n = 4) and SPECT (n = 1) procedures lowed by arm dysfunction (54%) and leg and foot disabili- comprised a control group (n = 5) that did not undergo ties (45%), compared with the unaffected side.10 Research operations and the surgical group (n = 21) that underwent suggests2,28 that after surgical treatment of pharmacologi- hemispherotomy (8 did not survive the procedure; 10 cally refractory epilepsy, the still immature brain tissue survivors underwent neural tract tracing, and 3 survivors has the potential to make an impressive recovery. Howev- underwent SPECT, comprising 13 rats for the surgical er, with respect to neural reorganization, the mechanisms group). Rats received an injection of the anterograde bio- of brain plasticity are still not well understood. tinylated dextran amine (BDA) neurotracer into the right In the field of experimental neurosurgery, research has cerebral hemisphere. BDA was microinjected into the been conducted to analyze the behavioral and clinical ef- primary motor cortex (M1) or into the nucleus caudatus/ fects of neurosurgical intervention on functional/morpho- putamen (CPu) according to stereotactic coordinates from logical adaptations of neural structures, resulting in neural Paxinos and Watson’s atlas (The Rat Brain in Stereotaxic reorganization and functional recovery after hemispher- Coordinates35) as follows: anteroposterior = 0.12 mm to ectomy and hemidecortication.29,45,49 These studies were M1 and 1.92 mm to the CPu, middle-lateral = 2.0 mm to based on animal models of surgical techniques using ro- M1 and 2.6 mm to the CPu, and dorsoventral = 5.8 mm to dents, felines, and primates (both young and adult labora- M1 and 5.0 mm to the CPu. The surviving animals (n = 4, tory animals). For example, several studies22,33,44 used cats control group; n = 10, surgical group) were killed 10 days and/or rats to investigate experimental models of focal after either neural tract tracing or tracing in addition to cortical seizure, performing amygdalohippocampectomy, hemispherotomy invasive procedures. callosotomy, and multiple subpial transections aimed at As noted above, 4 rats were selected from the groups epilepsy control by surgical intervention. in this study and submitted to functional imaging pro- Experimental neurological approaches investigate the cedures, distributed into two independent experimental complex neurobiological mechanisms involved in epilep- groups: 1) the control group (n = 1) and 2) the surgical togenesis and the maintenance of seizures,25 the develop- group (n = 3). Two weeks after the procedure, rats from ment of new antiepileptic drugs,9,18,20 alterations in synap- both groups (control and surgical) were anesthetized and tic plasticity,26,50 the neurophysiological and neuropharma- underwent the SPECT imaging technique (Fig. 1). cological bases of the postictal immobility syndrome,8,12 the characteristics of ictal and postictal states,31 and post- Neurosurgery: Experimental Hemispherotomy surgical recovery skills.5,40 None of these lines of research, The animals were placed individually in an induction however, are related to the resection of relevant cortical re- chamber (150 × 150 × 300 mm), and anesthesia was in- gions or disconnection of cortical tracts in animals under- duced with 5% isoflurane (Cristália Pharmaceutical and going acute and chronic models of generalized, multifocal, Chemical Products Ltd.) in 100% oxygen with a delivery or limbic epileptic induction and cortical reorganization. rate of 1 L/min until loss of righting reflex. Anesthesia The aim of the present work is to describe a new ex- was then maintained with isoflurane at 100% oxygen with perimental neurosurgical model of hemispherotomy in a flow of 1.5–2.0 L/min, administered by means of endo- young Wistar rats. The new surgical approach not only tracheal intubation and kept under controlled ventilation clarifies neuronal mechanisms underlying behavioral re- (CR-Bion). Each rat was treated with an intramuscular in- covery from early cortical injury, but also may open new jection of penicillin-G benzathine (120,000 UI; 0.1 ml), perspectives on further investigation into the plasticity of followed by subcutaneous injection of the analgesic and corticospinal pathways
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