i UNIVERSITY OF GHANA COLLEGE OF HEALTH SCIENCES ANTICONVULSANT EFFECT OF ETHANOLIC LEAF EXTRACT OF EHRETIA CYMOSA THONN (BORAGINACEAE) IN MURINE MODELS BY LARTEY RICHARD NELSON (10552293) A THESIS SUBMITTED TO THE SCHOOL OF GRADUATE STUDIES IN PARTIAL FULFILLMENT OF THE AWARD OF MASTER OF PHILOSOPHY DEGREE IN PHARMACOLOGY DEPARTMENT OF PHARMACOLOGY AND TOXICOLOGY JULY, 2018 University of Ghana http://ugspace.ug.edu.gh ii UNIVERSITY OF GHANA COLLEGE OF HEALTH SCIENCES SCHOOL OF PHARMACY ANTICONVULSANT EFFECT OF ETHANOLIC LEAF EXTRACT OF EHRETIA CYMOSA THONN (FAM: BORAGINACEAE) IN MURINE MODELS BY LARTEY RICHARD NELSON (10552293) A THESIS SUBMITTEDTOTHE SCHOOL OF GRADUATE STUDIES IN PARTIAL FULFILLMENT OF THE AWARD OF MASTER OF PHILOSOPHY DEGREE IN PHARMACOLOGY DEPARTMENT OF PHARMACOLOGY AND TOXICOLOGY JULY, 2018 University of Ghana http://ugspace.ug.edu.gh i University of Ghana http://ugspace.ug.edu.gh ii ABSTRACT Purpose: Ehretia cymosa is used locally in Ghana to treat epilepsy. To validate this anecdotal information with scientific data, the anticonvulsant effect of the ethanolic extract of the leaves of Ehretia cymosa was studied in murine models. Materials and Methods: The potential anticonvulsant activity of an ethanol extract of Ehretia cymosa (ECE) (30, 100, and 300 mg kg -1 ) was tested employing the acute pentylenetetrazole (PTZ)-, PTZ-induced kindling, picrotoxin-induced seizures and maximal electroshock (MES) in mice. The extract‘s effect on motor co-ordination and nociception was also tested using the rota- rod and the hot plate tests respectively. Acute and sub-chronic toxicity tests were also done to ascertain how safe the extract is in rodents. Results: This study showed that, the ethanolic extract of ECE possesses anticonvulsant effects in the various seizure threshold models used, except in the maximal electroshock seizure model. The latencies to the first myoclonic jerks were increased by ECE while both the duration and frequencies of seizures reduced significantly. There was however no effect on motor coordination even when highest dose of 300 mg kg -1 was used. No mortalities were recorded in the animals used during the period of this study. The ECE also did not have any significant effect on any of the serum biochemical parameters after the study. Conclusions: The ethanolic extract of the leaves of the Ehretia cymosa was found to possess anticonvulsant properties, and possibly acts through the GABAergic transmission pathway but has no muscle relaxant properties. The findings from this study, therefore, give scientific University of Ghana http://ugspace.ug.edu.gh iii credence to the traditional use of Ehretia cymosa to manage epilepsy. The 10-week oral administration of the extract of Ehretia cymosa under the prevailing laboratory conditions was found to be relatively safe in male Sprague–Dawley rats. University of Ghana http://ugspace.ug.edu.gh iv DEDICATION I dedicate this work to my wonderful parents, Mr. John Attuah Lartey (of blessed memory), and Mrs. Attuah Gloria Lartey. You have been a blessing in my life. University of Ghana http://ugspace.ug.edu.gh v ACKNOWLEDGMENT I wish to express my utmost gratitude to God for His continuous blessings and mercies throughout this study. My profound appreciation goes to my mentor and supervisor Dr. Patrick Amoateng. Thank you for your support, expert direction, guidance, and great life lessons that you have taught me. For the mentorship I have received, I must say you have inspired me to aim far and beyond. I also say a hearty appreciation to Dr Kennedy Edem Kukuia, my co-supervisor for his mentorship and guidance as well. I say a very big thank you to all senior members, all lecturers, and technical support staff of the Department of Pharmacology and Toxicology, for the immense encouragement and emotional support. To the Head of Department of Animal Experimentation, Noguchi Memorial Institute for Medical Research (NMIMR), Dr. Samuel Adjei, I am glad to have been allowed to work in such an august department. I have learned some technical skills that would be with me forever. I thank all the staff and technical workers, especially Mr. Ahedor Believe, for his selfless assistance and help during my work there. I am also grateful to the technical staff of the Pharmacognosy department of the School of Pharmacy of KNUST especially Mr. Osafo Asare for his help in the collection of my plant sample. I am also very thankful to my work colleague Ms. Authentia Sokpe who pushed me to complete this work when I felt like giving up. May the Almighty God bless you abundantly. To my parents, Mr. and Mrs. Lartey, may God continue to bless you. Thank you for your financial support and advice. A big thanks to my family, especially my sister Lily who has been a mother and friend to me throughout my work. To all my colleagues, thank you all for your encouragement and support. God bless you. To friends, family, strangers, and anyone who has contributed to the successful completion of this work, I say may the Lord richly bless you. University of Ghana http://ugspace.ug.edu.gh vi TABLE OF CONTENTS DECLARATION ................................................................................................................... ii ABSTRACT ........................................................................................................................... ii DEDICATION .......................................................................................................................iv ACKNOWLEDGMENT......................................................................................................... v LIST OF FIGURES ...............................................................................................................ix LIST OF TABLES .................................................................................................................xi ABBREVIATIONS ............................................................................................................. xii CHAPTER 1 INTRODUCTION ......................................................................................... 1 1.0 GENERAL INTRODUCTION ..................................................................................... 1 1.1 PROBLEM STATEMENT ........................................................................................... 4 CHAPTER 2 LITERATURE REVIEW .............................................................................. 7 1.2 EPILEPTIC SEIZURES ................................................................................................ 7 1.3 SEIZURES AND EPILEPSIES .................................................................................... 8 1.4 MECHANISMS OF EPILEPTOGENESIS ................................................................ 11 1.4.1 VOLTAGE-GATED SODIUM CHANNEL SUBTYPES AND EPILEPSY ...... 13 1.4.2 GABAA RECEPTOR SUBUNITS AND EPILEPSY .......................................... 14 1.5 DISEASE MODIFICATION AND ANTIEPILEPTOGENESIS ............................... 16 1.6 SIDE EFFECTS OF ANTIEPILEPTIC DRUGS ....................................................... 19 1.7 ANIMAL MODELS OF EPILEPSY .......................................................................... 23 1.7.1 CHEMOCONVULSANT MODELS ................................................................... 24 1.7.2 ELECTRICAL STIMULATION ......................................................................... 25 1.8 EHRETIA CYMOSA THONN BORAGINACEAE..................................................... 26 1.8.1 PLANT DESCRIPTION ...................................................................................... 26 2.6.2 TRADITIONAL USES ............................................................................................ 27 CHAPTER 3 MATERIALS AND METHODS ................................................................... 30 1.9 DRUGS AND CHEMICALS ..................................................................................... 30 1.10 PLANT COLLECTION ............................................................................................ 30 1.11 PREPARATION OF EXTRACT .............................................................................. 30 1.12 QUALITATIVE PHYTOCHEMICAL ANALYSIS ON CRUDE EXTRACT ....... 30 1.12.1 TEST FOR TANNINS ....................................................................................... 31 1.12.2 TEST FOR REDUCING SUGARS ................................................................... 31 1.12.3 TEST FOR SAPONINS ..................................................................................... 31 University of Ghana http://ugspace.ug.edu.gh vii 1.12.4 TEST FOR ALKALOIDS .................................................................................. 31 1.12.5 TEST FOR FLAVONOIDS ............................................................................... 32 1.12.6 TEST FOR STEROLS........................................................................................ 32 1.12.7 TEST FOR TERPENOIDS ................................................................................ 32 1.13 HANDLING OF ANIMALS .................................................................................... 32 1.14 IRWIN OBSERVATION TEST ............................................................................... 33 1.15 HOT PLATE TEST ................................................................................................... 34 1.16 SKELETAL MUSCLE EFFECTS OF ECE ............................................................. 34 1.16.1 ROTAROD TEST .............................................................................................. 34 1.17 ANTICONVULSANT EFFECT OF EHRETIA CYMOSA ....................................... 35 1.17.1 PENTYLENETETRAZOLE (PTZ)-INDUCED SEIZURES ............................ 35 1.17.2 PICROTOXIN-INDUCED SEIZURES ............................................................. 36 1.17.3 PENTYLENETETRAZOLE-INDUCED KINDLING ...................................... 36 1.17.4 MAXIMAL ELECTROSHOCK TEST.............................................................. 37 1.18 TOXICITY STUDIES .............................................................................................. 38 1.18.1 ANIMAL GROUPINGS AND EXTRACT ADMINISTRATION.................... 38 1.18.2 HISTOPATHOLOGY AND BIOCHEMICAL ANALYSIS ............................. 38 CHAPTER 4 RESULTS.................................................................................................... 40 1.19 PHYTOCHEMISTRY SCREENING ....................................................................... 40 1.20 IRWIN TEST ............................................................................................................ 40 1.21 EFFECT OF EXTRACT ON NEUROMUSCULAR ACTIVITY ........................... 41 1.21.1 ROTAROD ......................................................................................................... 41 1.21.2 HOT PLATE TEST ............................................................................................ 42 1.22 ANTICONVULSANT THRESHOLD TESTS ......................................................... 43 1.22.1 PTZ-INDUCED SEIZURE TEST ...................................................................... 43 1.22.2 PICROTOXIN INDUCED SEIZURE TEST ..................................................... 46 1.22.3 MAXIMAL ELECTROSHOCK TEST.............................................................. 48 1.22.4 PTZ KINDLING TEST ...................................................................................... 50 1.23 TOXICITY STUDIES .............................................................................................. 53 1.23.1 BIOCHEMICAL PARAMETERS ..................................................................... 53 1.23.2 HISTOLOGICAL EXAMINATION OF ISOLATED TISSUES ...................... 56 CHAPTER 5 DISCUSSION ............................................................................................. 60 University of Ghana http://ugspace.ug.edu.gh viii CHAPTER 6 CONCLUSIOS AND RECOMMENDATIONS ........................................ 68 1.24 CONCLUSION ......................................................................................................... 68 1.25 RECOMMENDATIONS .......................................................................................... 68 REFERENCES ..................................................................................................................... 70 University of Ghana http://ugspace.ug.edu.gh ix LIST OF FIGURES Figure 2.1: The ILAE 2017 classification of types of seizures (Robert S. Fisher, 2017) 10 Figure 2.2: A figure showing the process of epileptogenesis (Alyu & Dikmen, 2017) 12 Figure 2.3: A figure showing the mechanism of anti-epileptic drugs (Shih, Tatum, & A Rudzinski, 2013) 19 Figure 2.4: A clinical side effect of phenytoin manifesting as gingival hypertrophy (Khorsand & Saaveh, 2007) 23 Figure 2.5: An overview of models for specific types of epilepsy or epileptic seizures (Löscher, 2011) 26 Figure 2.6 An image of Ehretia cymosa Thonn (Boraginaceae) http://tropical.theferns.info29 Figure 4.1: Effect of Ehretia cymosa extract ECE 30, 100, and 300 mg kg -1 on neuromuscular coordination in mice in the rotarod test. Data are Mean ± SEM (n=5) 42 Figure 4.2: Effect of ECE (30, 100, 300 mg kg -1 ) on latency [time for which mouse remained on the hot plate (55˚C ± 0.1˚C) without licking or flicking of the hind limb or jumping in seconds. 43 Figure 4.3: Effect of ECE 30, 100, 300 mg kg -1 and phenobarbitone 3, 10, 30 mg kg -1 on the latency to first myoclonic jerks, the total frequency of the seizures, and total frequency of the seizures induced by PTZ. Each column represents the mean ± SEM (n = 5). *P < 0.05, **P < 0.01compared with vehicle-treated group (one- way analysis of variance followed by Newman–Keuls post hoc test). 45 Figure 4.4:Effect of ECE 30, 100, 300 mg kg-1 and phenobarbitone 3, 10, 30 mg kg-1 on the latencies to first myoclonic jerks, the total frequency of the seizures, and total frequency of the seizures induced by picrotoxin. Each column represents the mean ± SEM (n = 5). *P < 0.05, **P < 0.01compared with vehicle-treated group (one-way analysis of variance followed by Newman–Keuls post hoc test). 47 Figure 4.5: Effect of ECE 30, 100 and 300 mg kg -1 and carbamazepine 3, 10 and 30 mg kg - 1 on the duration of First HLE induced by Maximal Electroshock Test (MEST).49 University of Ghana http://ugspace.ug.edu.gh x Figure 4.6: Effect of ECE 30, 100 and 300 mg kg -1 and carbamazepine 3, 10 and 30 mg kg - 1 on the total duration of Hind Limb Extensions (HLE) induced by Maximal Electroshock Test (MEST). 50 Figure 4.7:The dose-response effects of ECE 30, 100, and 300 mg kg -1 (A and B) and phenobarbitone 3, 10, and 30 mg kg -1 (C and D) on the PTZ-kindled mice. 52 Figure 4.8: The Photomicrographs of Brain isolated from rats after 72-day continuous administration of (A) Vehicle, (B) ECE (30, 100 and 300 mg kg -1 ), (H&E staining, 40×). 56 Figure 4.9:The Photomicrographs of livers isolated from rats after 72-day continuous administration of (A) Vehicle, (B) 30 (C) 100 and (D) 300 mg kg -1 ) (H&E staining, 40×). 57 Figure 4.10:Photomicrographs of kidneys isolated from rats after 72-day continuous administration of (A) Vehicle, (B) ECE 30, (C) 100 and (D) 300 mg kg -1 showing normal renal tubule and glomeruli (H&E staining, 40×). 58 Figure 4.11:Photomicrographs of hearts isolated from rats after 72-day continuous administration of (A) Vehicle, (B) 30, (C) 100, (D) ECE 300 mg kg -1 ) showing normal myocardial fibers with characteristic central nuclei and branching arrangement as indicated by the arrows. 59 University of Ghana http://ugspace.ug.edu.gh xi LIST OF TABLES Table 4.1: Primary phytochemical screening of ECE 40 Table 4.2: IRWIN TEST RESULTS 41 Table 4.3: A table showing the biochemical analysis of a single administration of ECE (30, 100 and 300 mg kg -1 ) after a 72-day study period in Sprague-Dawley male rats54 University of Ghana http://ugspace.ug.edu.gh xii ABBREVIATIONS AED Antiepileptic drugs CBZ Carbamazepine CNS Central Nervous System DZP Diazepam ECE Ehretia cymosa Extract ED50 Effective dose for 50% EEG Electroencephalography GABA γ- aminobutyric acid GABA-T GABA Transaminase GAT1, GABA transporter 1 HLTE Hind limb Tonic extensions ILAE International League Against Epilepsy LD50 Lethal dose which causes the death of 50% MEST Maximal Electroshock Threshold test University of Ghana http://ugspace.ug.edu.gh xiii MRI Magnetic resonance imaging NMDA N-Methyl-D-aspartate PIC Picrotoxin PTZ Pentylenetetrazole SE Status epilepticus SV2A Synaptic vesicle protein 2A TLE Temporal lobe epilepsy VPA Valproic acid University of Ghana http://ugspace.ug.edu.gh 1 CHAPTER 1 INTRODUCTION 1.0 GENERAL INTRODUCTION Epilepsy is a disease condition that dates back to the very existence of mankind with references in ancient writings including the Bible (WHO, 2019; King James Version, Matthew 17:14-15). In the pre-Hippocratic era, the condition was however thought of as a retribution for offences committed. Thus, its treatment was sought in the temples (York, 2005). This can be seen where one man pleaded with the Messiah to cure his son who usually exhibited the symptoms of epilepsy (King James Version, Matthew 17:14-15). By the man‘s description, it can be inferred that he believed the disease had a spiritual cause and as such needed spiritual healing. The Messiah went ahead and healed the said boy who was described by the father as a lunatic; sorely vexed and often times fell into the fire (King James Version, Matthew 17:17 -18). However, Hippocrates, the father of medicine, disputed the mystical cause of epilepsy. To this, he said that the only reason men thought epilepsy was divine was that there was no understanding of the disease (York, 2005) Modern physicians also agree with this view. It is therefore incumbent on the scientist to explore the scientific dimension to the disease epilepsy. The International League Against Epilepsy (ILAE) defines epilepsy as a disease of the central nervous system (CNS) which is also characterized by seizures. The seizures are transitory, unprovoked, sudden, and recurrent episodes of abnormal hypersynchronous neuronal discharge. In other words, it is a brain condition which is associated with the occurrence of more than one epileptic seizure. There is also an increased susceptibility to generate more University of Ghana http://ugspace.ug.edu.gh 2 seizures in addition to psychological, cognitive, neurobiological and social disturbance (R S. Fisher et al., 2005). Epilepsies are classified into four groups namely: partial (focal) seizures, generalized seizures, combined generalized and focal, and the unclassified (unknown) seizures. Categorization of the condition is determined by the type of seizure. The partial type of seizures stem from networks linked to one hemisphere of the brain and this is usually accompanied by an underlying structural disease. On the other hand, generalized seizures originate from bilaterally distributed networks which lead to the concurrent start of extensive electrical discharge with no localizing characteristics referable to a single hemisphere (Wilkinson et al., 2017). The combined generalized and focal type are seizures which have characteristics of both focal and generalized types of seizures. The unknown epilepsy refers to one with little information on the clinical condition. The unknown type of epilepsy may be re- classified as focal, generalised or combined generalized and focal types of epilepsy if later enough clinical information becomes available (Chang, Leung, Ho, & Yung, 2017). Though epilepsy is one of the oldest documented conditions dating as far back as the year 4000 BC (WHO, 2019), successful cure has not been achieved. Thus, an estimated sixty-five (65) million still live with the condition and out of this number, the active epilepsy cases with recurrent seizures requiring regular treatment at any given time is estimated to be around 4 to 10 per 1000 people (in developed countries) and 7 to 14 in developing countries. In addition to this, the number of people that are estimated to be diagnosed with epilepsy each year from these countries is said to be around 2.4 million relative to 30 to 50 per every 100 000 people (Vogel, Franz, Jochen, & Dieter, 2015). University of Ghana http://ugspace.ug.edu.gh 3 To compound this worrying statistics, there is fear, discrimination, and social stigma attached to the disease and this can even be used as grounds to annul or prohibit marriages in some countries (Vogel et al., 2015). Aside from these, the treatment and management of epilepsy with various anticonvulsant drugs have a lot of side effects. Some of these unwanted effects such as aberrant gum growth (gum hyperplasia), hardening of the face, and excessive hair growth or hirsutism affect the physical appearance or the beauty of the patients. There are also recorded cases of cognitive impairment, hypersensitivity reactions, behavioural changes, and peripheral neuropathy. There are also issues like Dupuytren's contractures, gastrointestinal problems, hyponatremia, leukopenia, weight gain, and endocrine changes reported as side effects of taking some of these antiepileptic drugs. There is also the issue of tolerance and dependence associated with the use of antiepileptic drugs (Löscher & Schmidt, 2006). These effects are experienced depending on the type of medication being used to manage the condition (Vogel et al., 2015). The numerous adverse effects associated with anti-seizure drugs have negatively impacted the clinical effectiveness of the medications. Also, the socio-economical differences between the developed and developing world impact clinical outcomes largely. Epilepsy places a heavy economic burden on both patients and their countries. Consequently, it is pertinent to assess the treatment and management of epilepsy so as not to only to increase quality of life, but also consider the financial or economic burden of the prescribed treatments for this disease condition (Liu, Liu, & Meng, 2013). For these reasons, there should be a pragmatic research into novel plant-based medicines that are readily available and safer to use for the control of convulsions. University of Ghana http://ugspace.ug.edu.gh 4 Ehretia cymosa, known as Okusua in the Twi, is a shrub or small tree with drooping branches and can be found in the savannah, forest thickets, and cultivated lands (Mshana, 2000). The infusion of the leaves is used as a bath to manage fevers and convulsions. The roots are used to cure tetanus and dysentery, whereas the leaves are employed in the treatment of headaches, constipation in children, and fractures (Mshana, 2000). The hydroethanolic extract of the leaves has been reported to have antidiabetic, antimicrobial, and antioxidant properties (H. M. Burkill, 1985). Despite its folkloric use for convulsions, there is no scientific data confirming its anti-convulsant or antiepileptic properties. There is therefore the need to investigate its antiepileptic and related neuropharmacological properties as well as its safety. 1.1 PROBLEM STATEMENT An estimated 65 million people suffer from epilepsy worldwide and it is the most predominant cause of chronic neurological diseases. Even more frightening is that, about 30 percent of the people who live with epilepsy are unresponsive to clinical management (Łukawski et al., 2018). Unfortunately, a third of these people in this category live in Africa, and this accounts for nearly 16% of people afflicted globally. Furthermore, the problem is compounded by a wide treatment gap that can even be as high as 100 percent in some suburbs in the African region (Mugumbate & Zimba, 2018). People living with epilepsy have, throughout history, been associated with the divine, demonic, and supernatural attributes (Devinsky & Lai, 2008). The mystical associations with the disease coupled with poor scientific understanding of the disease have resulted in serious social implications for patients, University of Ghana http://ugspace.ug.edu.gh 5 especially for women due to the stigma attached to the condition (Kpobi, Swartz, & Keikelame, 2018). In addition to these, antiepileptic drugs (AEDs) have side effects and poor tolerability which greatly affects patients‘ compliance. Patients on antiepileptic drugs go through a strained social and emotional wellbeing due to physical changes like acne, alopecia, hirsutism and weight gain which in turn lead to a low quality of life (Chen et al., 2015). These side effects lead to increased drug non-adherence which in turn lead to reduced effectiveness of AED regimen leading to higher rates of road traffic accidents, injuries and fractures (Faught, Duh, Weiner, Guerin, & Cunnington, 2008). The consequence of this AED non- adherence is increased mortality rates and adverse clinical outcomes. This can lead to patients being incorrectly classified as having a refractory epilepsy (O‘Rourke & O‘Brien, 2017). In addition to these, non-adherent adults with epilepsy (AWE) are known to run the risk of developing convulsive status epilepticus (Skinner et al., 2010). The most serious outcome of AED non-adherence is the increased risk of sudden unexplained death in AWE (Lathers, Koehler, Wecht, & Schraeder, 2011). It is therefore imperative to identify the barriers to AED and remove those hurdles to enable a better management of this disease condition. Aside from the cosmetic side effects, some of the currently available anti-seizure drugs like felbamate, phenytoin and valproic acid have been implicated in liver toxicity (Vidaurre, Gedela, & Yarosz, 2017). With regards to primary health care, an estimated 80 percent of the worldwide population depend on herbal medicines (Sam, 2019) hence herbal medicines can be a good source of antiepileptic drugs that are easily accessible, able to prevent epileptogenesis and with few side effects. University of Ghana http://ugspace.ug.edu.gh 6 AIM This research seeks to investigate the anti-epileptic effect of the ethanolic extract of Ehretia cymosa. OBJECTIVES 1. To determine the effects of Ehretia cymosa extract on motor co-ordination and nociception. 2. Investigate the effect of the extract of Ehretia cymosa extract on convulsive threshold tests using the acute and chronic models of convulsion. 3. Perform acute, sub-acute, and sub-chronic toxicity tests. University of Ghana http://ugspace.ug.edu.gh 7 CHAPTER 2 LITERATURE REVIEW 1.2 EPILEPTIC SEIZURES Epileptic seizures are defined as transient occurrences of signs and/or symptoms as a result of excessive, aberrant or hypersynchronous neuronal brain activity (Falco-Walter, Scheffer, & Fisher, 2018). Approximately 65 million people in the world are affected by this condition (Ngugi, Bottomley, Kleinschmidt, Sander, & Newton, 2010) and the prevalence of this condition is around 6.4 cases per 1000 people according to data available (Fiest et al., 2017). Even though it is one of the most predominant and disabling neurologic diseases, there is still not a complete comprehension of the pathophysiology and proven treatment regimen to combat the condition (Stafstrom & Carmant, 2015). Case management of the condition is usually by the use of antiepileptic drugs. However, there are about one-third of such patients who do not attain seizure control with the available drugs (Devinsky et al., 2018). One of the most effective ways to help eliminate these seizures is through surgeries but only a small percentage of these patients are qualified for such surgeries (Wiebe, Blume, Girvin, & Eliasziw, 2001). A lot of the patients whose conditions have become drug-resistant are not eligible and the options available for such patients are the use of neurostimulation devices, adherence to the good dietary regimen, or partaking in clinical trials for new anti-seizure drugs (ASDs) (Wiebe et al., 2001) patients may relapse. An estimated 10 percent of the people in the world will experience a seizure at least once in their life (Hauser & Beghi, 2008). Epilepsy can lead to death directly through events like head injuries from falls, burns, drowning, vehicular accidents, sudden death that occurs in epilepsy and status epilepticus. There can be indirect causes like suicide, pneumonia, or through the adverse drug reactions of University of Ghana http://ugspace.ug.edu.gh 8 anti-seizure drugs like obesity and cardiovascular reactions (Devinsky, Spruill, Thurman, & Friedman, 2016). 1.3 SEIZURES AND EPILEPSIES Seizures are defined as paroxysmal change of neurologic function due to excessive, hypersynchronous neuronal discharge in the brain. It is usually unprovoked and recurrent and the cause can be attributed to an underlying brain disorder (Shorvon, Andermann, & Guerrini, 2011). When the cause of seizures is through reversible condition like fever or hypoglycemia, it is not considered epilepsy (Shorvon et al., 2011). Epilepsy syndrome on the other hand refers to a pattern of clinical manifestations that consistently occur together with seizures as a primary manifestation. Some of the features of an epilepsy syndrome include similar age of onset electroencephalogram (EEG) findings, etiology, inheritance pattern and response to particular antiepileptic drugs (Stafstrom & Carmant, 2015). Seizures are classified into 3 groups: generalized type seizures, focal type seizures which was formerly called partial, and epileptic spasms. Focal seizures stem from neuronal networks specific to one area of the cerebral hemisphere. Generalized seizures originate in bilateral distributed neuronal networks. A focal seizure can later become a generalized seizure. For an appropriate diagnosis to be made, a physician must combine a comprehensive history in addition to results from an electroencephalogram (EEG) and response to anti-seizure medications (Stafstrom & Carmant, 2015). Generalized seizures are classified as absence, generalized tonic-clonic, myoclonic and atonic seizures. Absence seizures which were formerly named petit mal is a type of seizure in which University of Ghana http://ugspace.ug.edu.gh 9 the patient stares into space for a few seconds and also becomes unresponsive to external verbal stimuli but blinks the eye or nods the head occasionally. Generalized tonic-clonic (GTC) seizures which were previously named grand mal comprise of bilateral symmetric convulsive movements in addition to the body becoming stiff. After this, jerking of all the limbs take place. There is no loss of consciousness during such an episode. In myoclonic seizures, there is an abrupt, short very fast movement that is not associated with any loss of consciousness. The muscle contractions associated with this kind of seizure are usually brief and involuntary and may impair one or several other muscles. For this reason, myoclonic seizures can either be classified focal type seizures or generalized type seizures. On the other hand, atonic seizures are characterized by body tone loss, which lead to a head drop or fall (Stafstrom & Carmant, 2015). When the brain has an imbalance between excitation (E) and inhibition (I), then, seizures can be said to be occurring (Rho, Sankar, & Stafstrom, 2010). The excitation/inhibition variation can be as a result of a change at various stages of the function of the brain from subcellular to genetic signaling cascades to general neuronal circuits. This imbalance can either have a genetic cause or can be acquired. The genetic pathological causes of this disease can be ubiquitous in nature. Again, cerebral injuries that are acquired are able to alter the circuit function, for example, change in the structure of the hippocampal circuitry due to persistent head injury or febrile seizures (Berkovic, 2015). Synaptic excitatory role matures before inhibitory function in a young brain leading to increased excitation and seizure generation. More so, due to the propensity of the neurotransmitter GABA to cause excitation instead of inhibition early in life (Ben-Ari, 2002; Pitkänen, Lukasiuk, Dudek, & Staley, 2015) it can be University of Ghana http://ugspace.ug.edu.gh 10 partly deduced the brains of the very young people are easily prone to having seizures (G. L. Holmes & Ben-Ari, 1998). Focal seizures can be classified based on a level of awareness. The term awareness is used as a substitute for consciousness because consciousness comprises many aspects that can be difficult to fully evaluate. The level of consciousness and awareness are therefore two of many possible features of a seizure, but they play an important role with regards to seizures (Robert S. Fisher, 2017). Awareness is basically, the knowledge of the environment and of self. The ability to determine awareness is a practical tool utilized to assess if consciousness level is compromised or not. It is therefore the awareness during a seizure, and not awareness of whether or not a seizure has occurred (Robert S. Fisher, 2017). Figure 2.1: The ILAE 2017 classification of types of seizures (Robert S. Fisher, 2017) University of Ghana http://ugspace.ug.edu.gh 11 1.4 MECHANISMS OF EPILEPTOGENESIS Epileptogenesis is the process through which a formerly functional normal brain changes such that it becomes biased towards the production of the aberrant electrical events which in turn result in chronic seizures. In other words, epileptogenesis is the process whereby there is growth and extension of tissue which is able to generate seizures that are spontaneous in nature, which ultimately result in an epileptic condition (Łukawski et al., 2018). Various mechanisms have been proposed to be the mode of initiation of the disease. The ability to prevent chronic epileptic disorder by using the necessary procedures would be touted as the most ideal goal in the clinical management of an epileptic condition but this, has not been successful to this day. Due to this, various clinical trials aimed at preventing chronic epilepsy have often yielded bleak, discouraging results (Di Maio, 2014). There are various antiepileptogenic drugs like eslicarbazepine and diazepam but the connection between inhibition of epileptogenesis and neuroprotection is not apparent (Łukawski et al., 2018). The ability to prevent epileptogenesis after brain injury is currently a challenge that is still unmet (Pitkänen & Lukasiuk, 2011). Research in animal models is currently the best source of information in the research into epileptogenesis. As a result, a lot of animal models are being researched into, to better understand the pharmacological and pathophysiological causes of the disease (Russo & Citraro, 2018). The process of epileptogenesis happens in three phases. It first of all starts with, causative injury or event; after which there is a latent period during which the alterations that were caused by the said injury also change the formerly normal brain into an epileptic brain. Lastly, the third phase follows and this is the point where the epilepsy becomes fully established and chronic. The best point in the epileptogenesis whereby University of Ghana http://ugspace.ug.edu.gh 12 various medical management can be utilized to stop the ultimate occurrence of a chronic epilepsy is at the latent period during which an acquired epileptogenesis is believed to coalesce (Goldberg & Coulter, 2013). Figure 2.2: A figure showing the process of epileptogenesis (Alyu & Dikmen, 2017) 2.3.1 THE EMERGING TARGETS AND NOVEL STRATEGIES FOR FUTURE TREATMENT The discovery of novel antiepileptic drugs which would help to better control patients‘ seizures may require a fundamental change in the strategies of drug development. Instead of randomly screening compound libraries, rational drug design could rather be based on scientific understanding of the pathophysiological mechanisms of ictogenesis of epilepsies. After this is achieved, new compounds can be made to target specific established epileptic brain defects, which can lead to the direct control of causative pathways without causing harm University of Ghana http://ugspace.ug.edu.gh 13 to the normal neuronal function. Aside this, there could also be the use of more innovative ways that mimic one or more characteristics of pharmacoresistance in humans and integrate them into epileptogenesis models thereby aiding in characterizing possible disease-modifying therapies (Brodie et al., 2011; Walker, White, & Sander, 2002). 1.4.1 VOLTAGE-GATED SODIUM CHANNEL SUBTYPES AND EPILEPSY Voltage-gated sodium channels (VGSCs) are necessary for the production and propagation of coordinated action potentials in the whole nervous system. For this reason, they are believed to have a vital part in alleviation and occurrence of epilepsy. There have been several genetic studies on people living with epilepsy and these have helped characterized several mutations of more than 700 among the genes that code for voltage-gated sodium channels validating the role they play in pathogenesis. Again, a lot of anti-seizure medications are known to act on VGSCs to reduce seizures (Czuczwar & Patsalos, 2001). VGSCs are imperatively necessary for moderating neuronal excitability and subsequently, network activity. They can be found all over the central neuron compartments and their population is increased at the nodes of Ranvier and axon initial segments (AIS). In myelinated neurons, the collection of voltage- gated sodium channels at the nodes of Ranvier is important, the increase of the speed of action potential transmission by saltatory conduction (Conti, Hille, Neumcke, Nonner, & Stämpfli, 1976; Kaplan et al., 2001). Research into the genetics of epileptic patients has found a vast number of mutations out of the genes known to encode for these ion channels. A significant amount of these mutations are in VGSC genes with most discovered in SCN1A, and fewer in University of Ghana http://ugspace.ug.edu.gh 14 SCN2A, SCN8A, and SCN1B (Herlenius et al., 2007; Mulley et al., 2005; Striano et al., 2006; Wallace et al., 1998). VGSCs are very important mediators of intrinsic neuronal and muscle excitability. Any aberrant activity is key to the pathophysiology of seizures, and a lot of widely used antiepileptic medications, like carbamazepine and phenytoin are known inhibitors of VGSC activity. Many of the known antiepileptic medications block the VGSC but the drugs currently available are mostly non-selective and as such do not utilize the discrete attributes of the brain channels. VGSC are thought to be found at various regions\on the neuronal membranes and populations. For this reason, other compounds can be produced that can target only sodium channel conformations and its subtypes studied to be over-expressed in epileptic tissue, in so doing, sparing normal neuronal function. Lacosamide is one example of a blocker of sodium channel with distinct attributes with regards to selectivity for a specific biophysical state or subunit but unfortunately have a lot of side effects (Brodie et al., 2011; Errington, Stöhr, Heers, & Lees, 2008; Remy et al., 2003). 1.4.2 GABAA RECEPTOR SUBUNITS AND EPILEPSY This is a ligand-gated ion channel receptor that has a centrally placed anion pore around which five separate protein subunits are arranged. The anion pore is permeable to bicarbonate and chloride ions. There are 19 GABAA receptor subunits discovered so far and it has been shown that the composition of the subunit can affect the pharmacology and physiology of the receptor (Garcia, Kolesky, & Jenkins, 2010). In the brain, the receptors of GABAA possess an age-adapted role. In its early development, they moderate excitatory activities which result in the trigger of signalling processes that are calcium-sensitive necessary for brain University of Ghana http://ugspace.ug.edu.gh 15 differentiation. They however transmit inhibitory signals during later phases of their development (ILAE, 2018). These inhibitory effects have been significantly utilized in the management of diseases where there is the need of silencing neuronal activity. The function and physiology in the brain of epileptic patient or a status epilepticus subject change according to literature available (ILAE, 2018) and as such may have an influence on the propensity to seizures. For this reason, many available anticonvulsants have GABAA receptors as their primary or secondary targets (Chang et al., 2017). Some of these drugs act by increasing GABAA receptor activity through direct interaction with the receptor for example barbiturates, carbamazepine and benzodiazepines. Others indirectly increase the available GABA such as valproate and vigabatrin (Czuczwar & Patsalos, 2001; Granger et al., 1995; P. Kumar, A. Jhanjee, & M. Bhatia, 2010; Meldrum & Rogawski, 2007; Quilichini, Chiron, Ben‐ Ari, & Gozlan, 2006). Furthermore, anticonvulsants such as topiramate, zonisamide, acetazolamide can inhibit carbonic anhydrase through the reduction of the depolarizing outcome of GABAA receptors (Davis, Penschuck, Fritschy, & McCarthy, 2000; Dodgson, Shank, & Maryanoff, 2000; Nishimori et al., 2005; Reiss & Oles, 1996). Barbiturates which are part of the examples of available GABAA receptor medications are relatively non-selective (Walker et al., 2002). The ability to produce drugs that are of subunit specificity could help avoid unwanted side effects which are related to non-selective modulation of GABAA. There are records for subunit-specific AED: like stiripentol which has been shown to preferentially activate α3-β3-γ2-containing receptors. Hence, the ability to have drugs that are GABAA selective and can specifically act on subunits studied to be upregulated in epileptic brain tissue, may demonstrate being efficacious against seizures with less unwanted drug reactions University of Ghana http://ugspace.ug.edu.gh 16 (Brodie et al., 2011; Brooks-Kayal, Shumate, Jin, Rikhter, & Coulter, 1998; Johnston, 2005; Stell, Brickley, Tang, Farrant, & Mody, 2003). 1.5 DISEASE MODIFICATION AND ANTIEPILEPTOGENESIS The recent antiepileptic medications generally manage ictogenesis, or the commencement of paroxysmal activity (Reiss & Oles, 1996). Due to these, various classes of AEDs act by suppressing excitability of neuronal activity by blocking sodium channels or increasing inhibitory GABAergic activity (Czuczwar & Patsalos, 2001; White, 1999). Both cognition and ictogenesis are moderated by excitability of neuronal activity. For this reason, using the normal methods of AEDs screening may be difficult to find drugs that are non-impairing. However, employing chronic animal models of epilepsy may be used to improve drug screening. Thus, by using kindled or genetically modified animals (Matagne & Klitgaard, 1998) it may be possible to find novel AEDs that prevent the neuronal hypersynchronization which leads to an ictal event, without obstructing normal neuronal excitability (Margineanu & Klitgaard, 2000). When a normal brain undergoes multiphase events which end up producing alterations that enhance the development of spontaneous seizures, we term it as epileptogenesis. This can be as a result of brain damage caused by things like head trauma (Golarai, Greenwood, Feeney, & Connor, 2001), growth (Goldberg et al., 2013), stroke (Margineanu & Klitgaard, 2000), infection (Golarai et al., 2001), or status epilepticus. Usually, brain damage does not immediately lead to seizures and this is a latency period that may last for weeks or even years. In these latency periods, the normal seizure thresholds are lowered due to continuous alterations to the brain which also subsequently lead to University of Ghana http://ugspace.ug.edu.gh 17 spontaneous seizures (Golarai et al., 2001; Santhakumar, Ratzliff, Jeng, Toth, & Soltesz, 2001). Immediately seizures start occurring, the epileptic disease state worsens. Each seizure then has the propensity to produce extra neuronal changes that may additionally reduce seizure threshold (Goddard, McIntyre, & Leech, 1969). Most anticonvulsants act by either reducing seizure frequency or duration of seizure by reducing neuronal excitation, but ideal antiepileptogenic agents would either block the first epileptogenic development or alter the epileptic disease state after the onset of seizure (McNamara, 1984). The ideal screening for antiepileptogenic drug action would be studies that have the ability to reduce changes in cellular network and molecular properties that happen during the process of epileptogenesis. The animal model that is mostly employed for assessing the anti-convulsive characteristics of AEDs is the focal kindling. In this model, initial exposure to repeated sub-convulsive stimulus ultimately evokes seizures (Albright & Burnham, 1980; Goddard et al., 1969; McNamara, 1984). Initially, stimuli in the kindling process only elicit short-duration after-discharges as a result of a synchronous neuronal discharge near the stimulation. Further kindling stimulation produces prolonged after-discharges involving larger brain compartments with the quick involvement of the limbic system. With longer and repeated stimuli, behavioural seizures accompany the after-discharges and become more complex. It takes a number of days or weeks before there can be an increased sensitivity to a formerly sub-convulsant stimuli which subsequently reach a peak during which the kindling stimuli result in seizures and after- discharges (McIntosh & Levy, 2021). Since kindled seizures are inducible and have durations and behavioural and electrographic characteristics, kindling can be employed as a screening method for anti-seizure effects that are characterized easily. Potential AEDs can be University of Ghana http://ugspace.ug.edu.gh 18 administered to animals that have been fully kindled and the consequence on electrographic and behavioural seizures measured (Teskey, 2020). Kindling is progressive in nature and for this reason, repeated seizures over time can cause a reduction in seizure thresholds. This may be similar to the process of human epileptogenesis. The long interval between trauma and seizure manifestation in posttraumatic epilepsy may be a reflection of a slow kindling process (Skinner et al., 2010). This idea is buttressed by the generation of generalized seizures in a patient undergoing electrical stimulation of the thalamus (Lathers et al., 2011). There is data showing that the current antiepileptic drugs have antiseizure properties but not antiepileptogenic ones (Suchomelova et al., 2006). In other words, the symptoms can be managed but the ultimate development of epilepsy is not affected. Contrary to this, the priority of management of epilepsy is the discovery of therapeutic agents that can prevent or correct the neuropsychological and neurological deterioration accompanied with chronic seizures or, even stop epilepsy in individuals who are at risk (Brodie et al., 2011; Walker et al., 2002). FIG 2.3 illustrates some of the mechanisms of some the antiepileptic medications. University of Ghana http://ugspace.ug.edu.gh 19 Figure 2.3: A figure showing the mechanism of anti-epileptic drugs (Shih, Tatum, & A Rudzinski, 2013) 1.6 SIDE EFFECTS OF ANTIEPILEPTIC DRUGS The core aim of the management of people with epilepsy is to completely abolish or significantly reduce frequency of seizures, reduce the unwanted side-effects of drug therapy and greatly enhance medical and neuropsychiatric comorbidities (Pitkänen, 2010) Anti- seizure drugs (ASDs) aim to subdue the development, severity and the propagation of epileptic seizures but these medications are to be taken up to 4 times a day for years, and sometimes for throughout one‘s lifetime (Faught et al., 2008; Ryvlin, Cucherat, & Rheims, 2011). Drug noncompliance to ASDs treatment is not uncommon and this usually results in University of Ghana http://ugspace.ug.edu.gh 20 the seizure relapse which in turn leads to increased mortality, injuries, and frequent hospital visits and admissions with added costs (Faught et al., 2008). Unlike other disorders, such as hypertension in which an 80% compliance is accompanied with good disease management, a single missed dose of an ASD can result in a fatal seizure (Devinsky et al., 2018). Antiepileptic drugs (AEDs) can effectively manage patients with epilepsy but there is usually treatment failure and poor drug compliance due to the numerous side-effects experienced by taking these AEDs. These side-effects can lead to about 25% of the patients discontinuing treatment (Kwan & Brodie, 2000; Perucca, Carter, Vahle, & Gilliam, 2009; Uijl et al., 2009) and this lead to a significant reduction in their quality of life (Luoni et al., 2011; Uijl et al., 2009). Some of the frequently reported adverse drug reactions of AEDs are fatigue, tremors, gastrointestinal symptoms and memory problems. While others too experience dizziness, osteoporosis, drowsiness, depression, changes to their weight, and nausea (Carpay, Aldenkamp, & Van Donselaar, 2005). The impact of these adverse effects may further necessitate the need for specialist care which brings additional financial burden to the patient (de Kinderen et al., 2014). A lot of adverse drug effects are reported with AEDs but the most prevalent is CNS effects. When the regimen of an antiepileptic drug fails, it can lead to untoward effects which may be due to drug intolerance or to inadequate seizure control also due to drug inefficacy or a combination of both (Kwan & Brodie, 2000). The AEDs are either a first-generation or a second generation. Examples of the first-generation are valproate, phenobarbital, phenytoin, carbamazepine and primidone. The second-generation AEDs offer better response over first-generation drugs nonetheless, either of them can cause significant adverse effects (Cramer, Fisher, Ben‐Menachem, French, & Mattson, 1999). Poorly managed University of Ghana http://ugspace.ug.edu.gh 21 or controlled seizures may lead to a combination of drug therapy which further leads to potential pharmacokinetic or pharmacodynamic interactions leading to greater side-effects than when monotherapy is used (Hirsch et al., 2004). There are situations where seizures are not adequately controlled or there can be an imbalance between the control of seizures and adverse effects. In such instances, there may have to be a discontinuation of the drug which leads the patient being put on a new drug with their unique side effects (Lawal, Ogunwande, Salvador, Sanni, & Opoku, 2014). Some of the cognitive effects experienced by patients include loss of memory, diminished intelligence, attention and language skills. Even though most AEDs can cause cognitive impairment, phenobarbital and topiramate have been reported to have the most effects on cognitive abilities. Furthermore, the same phenobarbital has been shown to cause mental slowing which studies have shown that this diminished cognitive ability improves once the medication is stopped. Exposure of children to phenobarbital leads to intelligence scores less than those taking valproate (Lawal, Opoku, & Ogunwande, 2015). Anxiety and depression are common among epileptic patients (Blumer, Montouris, & Hermann, 1995). When these conditions exist before the diagnosis of epilepsy, the said conditions may worsen subtly with treatment thereby making it difficult to recognize (Ohemu et al., 2014). Carbamazepine has known side effects such as impaired balance, leucopenia, diplopia, blurred vision and drowsiness (Wilkinson et al., 2017). There is also been vertigo and loss of coordination, aplastic anemia and agranulocytosis have also been reported (Pellock, 1987). Patients on lamotrigine can develop Stevens-Johnson syndrome or toxic epidermal necrolysis University of Ghana http://ugspace.ug.edu.gh 22 especially those on valproic acid. Other unwanted effects include photosensitivity, diplopia, blurred vision, agitation, tremors, aplastic anemia and vomiting. There are reports indicating patients on levetiracetam to develop psychiatric side effects such as depression and agitation and other side effects like blood dyscrasias, dyspepsia, drowsiness, diplopia whiles the teratogenic effects of sodium valproate has also been reported (Alyu & Dikmen, 2017) and can also cause tremors, thrombocytopenia, nausea, pancreatitis, hair loss, edema, and ataxia (McIntosh & Levy, 2021). Phenytoin has been removed as a first-line drug because of its numerous toxicity issues which include gum hyperplasia (fig. 2.4), nystagmus, diplopia, tremor, dysarthria, and ataxia (Teskey, 2020). It can also lead to a decrease in intellect, depression, acne, and gum hypertrophy. Patients taking this drug can also develop coarse facial features polyneuropathy and blood dyscrasias (Wilkinson et al., 2017). Aside from these, lacosamide has been found to cause dizziness and ataxia and may even increase the risk of suicidal thoughts in patients taking these medications for any indication (P. Kumar, A. Jhanjee, & M. S. Bhatia, 2010). University of Ghana http://ugspace.ug.edu.gh 23 Figure 2.4: A clinical side effect of phenytoin manifesting as gingival hypertrophy (Khorsand & Saaveh, 2007) 1.7 ANIMAL MODELS OF EPILEPSY Temporal lobe epilepsy (TLE) is mostly accompanied by variable and recurrent seizures and this make this neurological disorder very difficult to understand. More often than not, seizures in TLE are often resistant to anti-epileptic medications. There is the option of resection of the epileptogenic tissue surgically but it is expensive and at times unfeasible. For these reasons, animal models that mimic the neuropathological, behavioural and electroencephalographic attributes of epilepsy have been developed and researched into in the past decades to better understand the pathophysiology of TLE and to also help develop better AEDs (York, 2005). Understanding epileptogenesis and seizure generation as well as their complex mechanisms in temporal lobe epilepsy and other forms of epilepsy is not completely possible in human clinical studies. Because of this, there has to be the use of appropriate animal models which will aim to mimic the symptoms of focal epilepsy with an epileptogenic injury or insult. The University of Ghana http://ugspace.ug.edu.gh 24 research into seizure mechanisms can give a better knowledge about the general functions and consciousness of the brain. Thus animal models can help with the advancement of the research into both neurophysiology and epilepsy (Löscher & Schmidt, 1988). FIG. 2.5 shows some of the various animal models employed in the discovery of antiepileptic medications. 1.7.1 CHEMOCONVULSANT MODELS Research into the chemoconvulsant pentylenetetrazole (PTZ) started in the later part of 1940s and continued through the early 1950s. During this period, properties of PTZ seizure threshold model were described by various publications, and this helped to make a comparison between the anticonvulsant attributes of antiepileptic medications (AEDs) in the PTZ and other animal models. This lead to the PTZ model being used in addition to other various animal models to discover most of the drugs currently utilized in epileptic seizure management (Yadeta, 2016). PTZ is believed to employ an antagonistic mechanism at the picrotoxinin-sensitive site at the GABAA receptor complex (Stegaroiu, 2016). Furthermore, (Bourgeois, 2014) has shown that PTZ and picrotoxin interact with distinct overlapping regions of the GABAA receptor. Chemoconvulsants are compounds that activate seizures and they can be employed in assessing various AEDs that act on different types of seizures. For example, compounds like N-methyl-D, L-aspartate and strychnine have been shown to trigger generalized tonic-clonic seizures, whereas PTZ generates non-convulsive myoclonic or absence seizures (Porter et al., 1984). Through these models, drugs like trimethadione, ethosuximide, valproate, and other efficacious medications have been discovered (Liu et al., 2013). Administrations of several University of Ghana http://ugspace.ug.edu.gh 25 doses of flurothyl or PTZ have also been employed to imitate recurrent generalized tonic- clonic seizures in young rodents (Pitkänen, Buckmaster, Galanopoulou, & Moshé, 2017). A single administration of PTZ can induce seizures and when it is given in sufficient amounts, status epilepticus can even be induced (Gregory L Holmes, Sarkisian, Ben‐Ari, & Chevassus‐ Au‐Louis, 1999; Pitkänen et al., 2017). 1.7.2 ELECTRICAL STIMULATION To better understand the mechanisms underlying epileptogenesis and ictogenesis, various animal models of seizures and epilepsy have contributed immensely to this effect. Furthermore, these models have played a significant part in the preclinical development and discovery of new antiepileptic drugs (AEDs) (Löscher, 2011). A lot of animal models of chronic brain disorders that are known to elucidate the pathophysiology of epilepsy and some of these chronic models of epilepsy are the kindling model of temporal lobe epilepsy (TLE), post-status models of TLE and genetic models of different types of epilepsy. Furthermore, ―the results from these models can be used to assess the effects of antiepileptic medications. A differentiation of the study of chronic models with models of acute seizures in previously healthy animals is the maximal electroshock seizure test. This can aid in testing of drugs in chronic models of epilepsy to provide data which is more predictive of clinical efficacy and unwanted drug reactions. Given this, chronic models can be employed early in the development and discovery of drugs to help reduce false positives (Loscher, 2002). University of Ghana http://ugspace.ug.edu.gh 26 Figure 2.5: An overview of models for specific types of epilepsy or epileptic seizures (Löscher, 2011) 1.8 EHRETIA CYMOSA THONN BORAGINACEAE 1.8.1 PLANT DESCRIPTION Ehretia cymose (see fig. 2.6) is a small tree that belongs to the Boraginaceae or borage family. It is found over a wide area of habitat throughout central, eastern, and western Africa, including Ghana, Côte d'Ivoire, Benin, Cameroon, Ethiopia and Kenya (Wikipedia Contributors, 2018, June 19). The plant is referred to as Okosua by the Akan-Twi speaking University of Ghana http://ugspace.ug.edu.gh https://en.wikipedia.org/wiki/Boraginaceae https://en.wikipedia.org/wiki/Borage https://en.wikipedia.org/wiki/Africa https://en.wikipedia.org/wiki/C%C3%B4te_d%27Ivoire https://en.wikipedia.org/wiki/Benin https://en.wikipedia.org/wiki/Cameroon https://en.wikipedia.org/wiki/Ethiopia https://en.wikipedia.org/wiki/Kenya 27 tribes from Ghana (Humphrey Morrison Burkill, 1985). The leaves of the plant are used among the people of south western Nigeria for the treatment of measles (Oladunmoye & Kehinde, 2011). The leaves have also been reported to be used for the management of epilepsy, spasms and convulsions, as a laxative, febrifuge, analgesic and for paralysis (H. M. Burkill, 1985). It is a small to medium deciduous tree or shrub that can grow up to 20 to 25 m tall. It has low and crooked branches that can grow up to up to 30 cm in diameter. The surface of the bark is grey to pale brown, with protruding lenticels. The leaves are spirally arranged and are simple and entire without any stipules present. The petiole is 1 to 3.5 cm long with an elliptical blade that is slightly grooved (Lemmens, 2009). It grows up to 7 m tall in the western parts but can grow as tall as 20 to 25 m as recorded in some parts of Southern Nigeria and Guinea. The fruit is normally black in colour, ovoid to globose drupe which is about 2-6 mm long (Harris & Harris, 2002). It has greyish brown wood with alternate lighter and darker bands (Conti et al., 1976). The main types of compounds identified in its volatile oils are fatty acids, sesquiterpenes, monoterpenes, , alcohols, phenylpropanoids and esters, (Jeruto, Mutai, Lukhoba, & Ouma, 2011). Its volatile oils have been demonstrated to have biological properties like cytotoxicity, insecticidal and antimicrobial activities (Lawal et al., 2014; Lawal et al., 2015). 2.6.2 TRADITIONAL USES The leaf of Ehretia cymosa is used in Ghana to treat fractures and to also enhance bone modelling. The leaves of the plant are used for treating headaches and fevers and also used for its mild laxative effects (Dalziel, 1937; Lewis & Avioli, 1991). Chewing sticks are made out University of Ghana http://ugspace.ug.edu.gh 28 of the branches for maintaining good gum and teeth hygiene (H. M. Burkill, 1985; Lewis & Avioli, 1991). An infusion of the leaf is used as a wash to treat convulsions, muscle spasms and fever (Borokini & Omotayo, 2012). The sap of the leaf is reported to be a mild laxative and can also be used as a hemostatic. Decoctions from the leaves are used to treat muscle stiffness, fevers and toothache. The twigs of the leaves are used in combination with other parts of plants to treat gastric ulcers whiles the decoctions of the leaf are used to cure dysentery and tetanus. The roots and leaves have been reported to be used as aphrodisiacs (Jeruto et al., 2011). Decoctions of the roots and bark are used to manage menstrual problems while a decoction of the bark alone is externally used to cure skin conditions. The people from Maasai treat brucellosis with the roots which are crushed in water and used against stomach diseases. Ehretia cymosa also serves locally as an important feed for livestock and in agroforestry in Ethiopia, it is sometimes planted as ornamental trees (Lemmens, 2009). The tree has several uses, providing food, wood and medicines for the local population of South Western Nigeria (Mulley et al., 2005). There is reported use of the leaves for the management of viral conditions like measles among the Southern Western people of Nigeria (Mulley et al., 2005). The decoction of the bark is used to regularize menstrual cycle and also treat pneumonia (Bankole et al., 2016; Ohemu et al., 2014). There is also reported use of the plant for the management of mental problems, venereal diseases, dry cough, malaria and tonsillitis, (Jeruto, Tooa, Mwamburia, & Amuka, 2015). University of Ghana http://ugspace.ug.edu.gh 29 Figure 2.6 An image of Ehretia cymosa Thonn (Boraginaceae) http://tropical.theferns.info University of Ghana http://ugspace.ug.edu.gh 30 CHAPTER 3 MATERIALS AND METHODS 1.9 DRUGS AND CHEMICALS This study employed the use of various chemicals including pentylenetetrazole, picrotoxin, phenobarbitone sodium, carbamazepine (Sigma-Aldrich Inc., St. Louis, MO, USA); 1.10 PLANT COLLECTION The leaves of Ehretia cymosa were harvested from Kwahu Asakraka (6.62942N6˚37'45.9048'', -0.68647W0˚41'11.30253'') in the Eastern Region of Ghana, and authenticated at the Pharmacognosy Department, KNUST and a specimen with voucher number, KNUST/2020/MN1/L009, was stored at the herbarium of the Faculty of Pharmacy, KNUST. 1.11 PREPARATION OF EXTRACT The leaves of the plant were powdered and serially extracted with 70% ethanol over 48 hours using a Soxhlet apparatus and concentrated under reduced pressure at 40-60 o C to a dark brown syrupy mass in a rotary evaporator. A water bath was used to dry resulting syrup mass and stored in a desiccator. The resulting extract was named Ehretia cymosa extract or ECE. 1.12 QUALITATIVE PHYTOCHEMICAL ANALYSIS ON CRUDE EXTRACT Screening of the extract to detect the presence of phytochemical constituents such as glycosides, tannins, sterols, alkaloids, terpenoids, saponins and flavonoids was done using procedures described by Evans and Trease (2009). University of Ghana http://ugspace.ug.edu.gh 31 1.12.1 TEST FOR TANNINS This was done by taking a quantity of 0.2 g of the extract which was dissolved in 25 mL of water and the resulting volume was topped up to 25 mL. A 1 mL aliquot of the extract was then added to 10 mL of water and 2 drops of 1% ferric chloride which produced the appearance of blue-black or green precipitate (ppt). 1.12.2 TEST FOR REDUCING SUGARS Twenty milligrams of the extract were warmed with 5 mL dilute H2SO4 on a water bath for 2 minutes and allowed to cool and filtered. Four drops of 20 % NaOH were added to the resulting filtrate after which 1mL volume of Fehling`s A and B solutions were added to the filtrate. It was then warmed and a red-brown ppt was then observed. 1.12.3 TEST FOR SAPONINS About 0.2 g of each extract was taken and shaken vigorously with about 10 mL of water for about one minute in a stoppered test tube and later the presence of a persistent froth was then observed. 1.12.4 TEST FOR ALKALOIDS Ten milliliter of dilute HCl was boiled with 0.2 g of the extract for 5 minutes. The resulting supernatant was then filtered into a separate test tube. About 3 drops of Dragendorff`s reagent was added to one milliliter of the filtrate and shaken together the appearance an orange spot ppt, was then observed. University of Ghana http://ugspace.ug.edu.gh 32 1.12.5 TEST FOR FLAVONOIDS A volume of 10 mL of 98% ethanol was added to 0.2 g of the extract. A small amount of zinc metal was then added followed by the drop-wise addition of concentrated HCl. The filtrate was then examined for the appearance of colors ranging from orange to red representing the presence of flavones, orange to crimson indicating flavonols, and crimson to magenta indicating presence of flavanones. 1.12.6 TEST FOR STEROLS Two milliliter of chloroform was added to 0.2 g and filtered. An amount of 0.2 g of the extract was added to 2 mL of chloroform and filtered. A volume of 2 mL of acetic anhydride was added to 1 mL of the filtrate after which few drops of concentrated H2SO4 was carefully added along the sides of the test tube. Violet to blue coloration which was produced indicated the presence of sterols. 1.12.7 TEST FOR TERPENOIDS An amount of 0.2 g of the extract was added to 2 mL of chloroform in a test tube followed by the addition of 1 mL of concentrated H2SO4. A reddish-brown coloration at interface indicated the presence of terpenoids. 1.13 HANDLING OF ANIMALS Sprague-Dawley rats (150-200 g) and Institute of Cancer Research (ICR) mice (20 – 25 g) were obtained from the Animal Department of Noguchi Memorial Institute for Medical University of Ghana http://ugspace.ug.edu.gh 33 Research, University of Ghana, Legon and kept in their Animal Experimentation labs. The animals were housed in cages with wood shavings as bedding and fed with standard mice chow, given water ad libitum. All animal procedures and techniques used in these studies were done under the Noguchi Institute of Animal Care and Use Committee (NIACUC) guidelines with a reference number 2017-05-2R. 1.14 IRWIN OBSERVATION TEST Irwin observation test is usually employed to evaluate the effects of a new substance on the physiological and behavioural function of experimental animals. The results obtained from the this test gives an insight into potential toxicity and enables doses to be selected for specific neuropharmacological investigation (Vogel et al., 2015). In this study, mice were grouped (n=5) and made to acclimatize for 24 hours before the start of the experiment. The laboratory mice were given the extract and compared with a control group given distilled water 10 mL kg -1 , p.o. The effect of the extract was evaluated at 6 doses; 10, 30, 100, 300, 1000, and 3000 mg kg -1 administered p.o. immediately before the test. Observations were performed 15, 30, 60, 120, and 180 minutes after administration of the extract and 24 and 48 hours later. Changes in physiological, behavioural and neurotoxicity symptoms, pupil diameter and rectal temperature were observed and recorded according to a standardized observation grid derived from that of Irwin (Biney, Mante, Boakye-Gyasi, Kukuia, & Woode, 2014; Irwin, 1968). University of Ghana http://ugspace.ug.edu.gh 34 1.15 HOT PLATE TEST The mice were weighed individually and made to acclimatize for 24 hours before the commencement of the experiment during which they were not given any food except for water. This is due to the fact that some food substances might have analgesic effect. The animals were put into 4 groups (n=5). These mice were pre-treated with the extract of Ehretia cymosa at 3 doses 30, 100 and 300 mg kg -1 p.o., and control of normal saline 10 mL kg -1 . After 60 minutes of pre-treatment, the animals were placed on a hot plate and the latency time which is the time for which mouse remains on the hot plate at (55˚C ± 0.1˚C) without licking or flicking of the hind limb or jumping was then recorded. A cut-off time of 30 seconds was the time limit for all the animals and this was done to prevent damage to tissues. The readings were taken after 0, 30, 60, 90, and 120 min post-administration of the test drug. The percentage analgesia was calculated using the following formula (Naveed, 2014).; – – – * 100 1.16 SKELETAL MUSCLE EFFECTS OF ECE 1.16.1 ROTAROD TEST Some test substances with anticonvulsant effect may impair motor coordination. This can be an important factor in the testing for anticonvulsant activity. The experiment was done to ascertain the effect of ECE motor coordination. Mice were randomly put into four groups (n=5) and trained to remain on a rotating rod (Ugo-Basile model 7600, Comerio, VA, Italy), rotating at 25 revolutions per min for 180 s over three days. This is referred to as habituation. . The actual study took place 24 hours after the last habituation during which the animals were University of Ghana http://ugspace.ug.edu.gh 35 given ECE 30, 100 and 300 mg kg -1 and distilled water 10 mL kg -1 p.o. after which they were put on the rotating rod and the latency of the mice to fall off the rotating rod within the stipulated time of 180 s was determined one-hour post-treatment. 1.17 ANTICONVULSANT EFFECT OF EHRETIA CYMOSA 1.17.1 PENTYLENETETRAZOLE (PTZ)-INDUCED SEIZURES Clonic-tonic seizures were induced in drug/vehicle pre-treated male Institute of Cancer Research (ICR) mice (20-30 g) by subcutaneous injection of 75 mg kg -1 pentylenetetrazole (PTZ) into the loose skin fold on the back of the neck of the mice. The animals were pre- treated with ECE (30, 100, and 300 mg kg -1 ) or phenobarbitone sodium (3, 10, 30 mg kg -1 ) thirty minutes before the injection of PTZ. The control animals received 0.9 % saline solution (10 mL kg -1 ). After the PTZ injection, the animals were placed in a testing chamber (made of perspex of dimensions 15×15×15 cm). A mirror angled at 45˚ below the floor of the chamber allowed a complete view of the convulsive event of PTZ. The behavior of the animals was captured with a camcorder (EverioTM model GZ-MG 130U, JVC, Tokyo, Japan) placed directly opposite to the mirror. The video recordings were later analyzed by tracking parameters including latencies to myoclonic jerks and clonic-tonic seizures and the duration of clonic-tonic seizures using Behavior Tracker Version 4.0 for Windows. The ED50 (a measure of anticonvulsant potency) was calculated by plotting the percent seizure inhibition of the drug to the vehicle-treated group. The ability of the drug or extract to prevent the University of Ghana http://ugspace.ug.edu.gh 36 seizures or prolong the latency of onset of the hind-limb tonic extensions was used as an indication for anticonvulsant activity‖. 1.17.2 PICROTOXIN-INDUCED SEIZURES Clonic-tonic seizures were induced in drug or vehicle pre-treated male ICR mice (20-30 g) by an intraperitoneal injection of 3 mg kg -1 picrotoxin (PIC). The mice were pre-treated with ECE (30, 100, 300 mg kg -1 ), or phenobarbitone sodium (3, 10, and 30 mg kg -1 ) thirty minutes before the injection of PIC. The control animals received distilled water (10 mL kg -1 , p.o). After the PIC injection, the animals were put in a testing chamber and a video recording of the event made. The video recordings were also later analyzed by tracking parameters including latency to myoclonic jerks and clonic-tonic seizures and the duration of clonic-tonic seizures using Behavior Tracker version 4.0 for Windows. The ED50 was calculated as indicated in the PTZ test. The mortality rate was also determined for each drug treatment group. The ability of a drug/extract to prevent the seizures or delay/prolong the latency of onset of the hind-limb tonic extensions was considered as an indication of anticonvulsant activity. 1.17.3 PENTYLENETETRAZOLE-INDUCED KINDLING To kindle the mice to spontaneous seizures, 35 mg kg -1 of PTZ was injected i.p. every 48 h into saline-, ECE- or phenobarbitone-treated male ICR mice (20-30 g). After the PTZ injection, the rats were placed in a testing chamber (made of perspex of dimensions 15×15×15 cm 3 ). A mirror angled at 45˚ below the floor of the chamber allowed a complete view of the convulsive event of PTZ. The behavior of the animals was captured with a camcorder (JVC University of Ghana http://ugspace.ug.edu.gh 37 Hard Disk Camcorder, GZ-MG 130U) placed directly opposite to the mirror. Seizure intensities were classified according to the Racine score (Racine, 1972) as follows: Stage 0: no response Stage 1: ear and facial twitching Stage 2: convulsive waves throughout the body Stage 3: myoclonic jerks, rearing Stage 4: turning over onto one side Stage 5: turning over onto the back, generalized tonic-clonic seizures Also, the latency to the onset of myoclonic jerks was measured and analyzed. Each rat was considered fully kindled after showing stage 4 or 5 after two consecutive PTZ administrations. On day seven after kindling had been achieved, the rats were challenged with 35 mg kg -1 of PTZ and the entire event was also recorded. The ED50 was then calculated. 1.17.4 MAXIMAL ELECTROSHOCK TEST The experiment employed the use of male ICR mice put into seven groups (n=10). Out of these, three of the groups were treated with the extract (10, 30, and 100 mg/kg, p.o.). Three other groups were treated with carbamazepine (10, 30, and 100 mg/kg, p.o.). The last group served as the control and they were administered distilled water (10 mL/kg, p.o.). The convulsions were then induced in the mice after 1 hour of drug pre-treatment. This was done by passing alternating electrical current (50 Hz, 60 mA, and 0.2 s) through the electrodes University of Ghana http://ugspace.ug.edu.gh 38 attached to the earlobe of the mice. After this, the duration of tonic hind limb extension seizures was determined in each dose group (K. E. Kukuia et al., 2012). 1.18 TOXICITY STUDIES 1.18.1 ANIMAL GROUPINGS AND EXTRACT ADMINISTRATION The Sprague-Dawley rats were randomly put into four groups (n=10); namely; control group (normal saline 10 mL kg -1 ), ECE 30, 100, and ECE 300 mg kg -1 doses and made to acclimatize for 5 days. The animals were subsequently given a daily dose of the test substances for 72 days by oral gavage. This was done to mimic the traditional folkloric route of administration. All drug administrations were given at 8:00 GMT each day and the blood collection and post-mortem examinations were done before 15:00 GMT. 1.18.2 HISTOPATHOLOGY AND BIOCHEMICAL ANALYSIS 1.18.2.1 PREPARATION OF SPECIMEN All animals were sacrificed and their organs (liver, kidney, lungs, spleen, heart, and brain) were harvested and placed in labelled containers containing 10% neutral buffered formalin. The organs were transported to the pathology laboratory of School of Dentistry, Korle-bu for processing and examination. Blood was collected from the jugular vein into serum separating gel tubes (BD Vacutainer® blood collection Tube Product, USA) and ethylene diamine-tetracetate (EDTA) tubes (Mediplus vacutainer K3, Sunphoria Co. Ltd., Taiwan) for serum preparation and haematological analysis respectively. Values for the level liver transaminases (AST, ALT, University of Ghana http://ugspace.ug.edu.gh 39 ALP), total protein (TP), direct bilirubin (D. Bilirubin) indirect bilirubin (Indi. Bilirubin), total bilirubin (T. Bilirubin), triglycerides and albumin in the serum were measure. Also, the levels of kidney urea (Ur), creatinine (Cr), lipid profile (HDL, LDL, total cholesterol) were calculated. These were done using an automated clinical chemistry analyzer (ABX Pentra C200, Horiba Medical, USA). 1.18.2.2 PROCESSING OF TISSUES Portions of the organs were selected into labelled tissue processing cassettes and processed into paraffin blocks. Each was passed through ascending grades of alcohol (70%, 80%, 90%, and absolute) and further two changes of absolute alcohol for dehydration, cleared in three changes of xylene, and finally infiltrated and embedded in paraffin wax. Five-micron sections were cut from each block, mounted on microscope slides and stained using the haematoxylin and eosin. University of Ghana http://ugspace.ug.edu.gh 40 CHAPTER 4 RESULTS 1.19 PHYTOCHEMISTRY SCREENING Phytochemical analysis of the leaf extract of Ehretia cymosa (ECE) (Table 4.1) revealed the presence of these plant secondary metabolites: tannins, saponins, terpenes, triterpenes, phenolic compounds, flavanoids, volatile oils, steroids, and glycosides. Alkaloids were however absent. Table 4.1: Primary phytochemical screening of ECE PHYTOCHEMICAL REMARK Tannins + Glycosides + Alkaloids - Flavonoids + Terpenoids + Saponins + Volatile Oils Phenolic compounds + + (+) Present (-) Absent 1.20 IRWIN TEST No death was recorded after 48 h, thus LD50 was estimated to be greater than 3000 mg kg -1 (Table 4.2). This test provided the dose ranges (30, 100, and 300 mg kg -1 ) for the actual work. University of Ghana http://ugspace.ug.edu.gh 41 Table 4.2: IRWIN TEST RESULTS Dose (mg/kg) Mortality Latency (min) Observed drug effects 10 0 15-120 Sedation, urination, defecation, 30 0 15-120 Sedation, urination, defecation, analgesia 100 0 15-180 Sedation, urination, defecation, analgesia 300 0 15-180 Sedation, urination, defecation, analgesia 1000 0 15-120 Sedation, urination, defecation, analgesia, altered respiration, tremors 3000 0 15-120 Sedation, urination, defecation, analgesia, altered respiration Saline 0 15-30 urination, defecation 1.21 EFFECT OF EXTRACT ON NEUROMUSCULAR ACTIVITY 1.21.1 ROTAROD The extract, Ehretia cymosa (30, 100, 300 mg kg -1 ), did not have any significant effect (F3, 16=0.3460 P=0.7925) on time spent on the rotating rod when compared to saline group (Figure 4.1). University of Ghana http://ugspace.ug.edu.gh 42 Figure 4.1: Effect of Ehretia cymosa extract ECE 30, 100, and 300 mg kg-1 on neuromuscular coordination in mice in the rotarod test. Data are Mean ± SEM (n=5) 1.21.2 HOT PLATE TEST The latency time (time for which mouse remained on the hot plate (55˚C ± 0.1˚C) without licking or flicking of the hind limb or jumping) was recorded. The ECE extract could not significantly increase the latency (F 3, 8 =2.907 P=0.1011) as compared to the control (Figure 4.2). Vehicle 30 100 300 0 500 1000 1500 2000 ECE (mg/kg) R o ta ro d A U C University of Ghana http://ugspace.ug.edu.gh 43 Figure 4.2: Effect of ECE (30, 100, 300 mg kg -1 ) on latency [time for which mouse remained on the hot plate (55˚C ± 0.1˚C) without licking or flicking of the hind limb or jumping in seconds. Each column represents the mean ± SEM (n = 5). 1.22 ANTICONVULSANT THRESHOLD TESTS 1.22.1 PTZ-INDUCED SEIZURE TEST The test employed pentylenetetrazole (75 mg kg -1 s.c) which induced myoclonic convulsions in all animals pre-treated with normal saline (10 mL kg -1 ). Ehretia cymosa 30, 100 and 300 mg kg - 1 reduced the duration of tonic convulsions significantly; fig 4.3C (P= 0.0024; F 3, 16 = 7.491). In the ECE treated animals, the frequency of convulsions was progressively and significantly reduced at all three doses 30, 100 and 300 mg kg -1 fig. 4.3B (P= 0.0031; F 3, 16 = 7.069). There was an observed significant (P<0.0001, F3, 16 = 2.797) increase in latency to the first myoclonic jerk fig. 4.3A, with statistical significance at doses 30 mg kg -1 (P= 0.0031; F 3, 16 = 2.797). Phenobarbitone on the other hand which was used as a reference anticonvulsant produced a dose-dependent increase in latency to the first myoclonic jerk for the 3 and 30. It significantly Veh 30 100 300-30 -20 -10 0 10 20 30 ECE ( mg/kg) L at en cy ( s) University of Ghana http://ugspace.ug.edu.gh 44 delayed the onset (F3, 16=5.285, P=0.0100) and reduced the frequency (F3, 16=7.069, P=0.0031) and duration (F3, 23=4.177, P=0.0231) of PTZ-induced convulsions (Figure 4.3). University of Ghana http://ugspace.ug.edu.gh 45 Figure 4.3: Effect of ECE 30, 100, 300 mg kg -1 and phenobarbitone 3, 10, 30 mg kg -1 on the latency to first myoclonic jerks, the total frequency of the seizures, and total frequency of the seizures induced by PTZ. Each column represents the mean ± SEM (n = 5). *P < 0.05, **P < 0.01compared with vehicle-treated group (one-way analysis of variance followed by Newman–Keuls post hoc test). University of Ghana http://ugspace.ug.edu.gh 46 1.22.2 PICROTOXIN INDUCED SEIZURE TEST The picrotoxin (3 mg kg -1 ) experiment induced generalized tonic-clonic convulsions in all animals treated. ECE 30, 100, 300 significantly; fig. 4.4C (F3, 16=12.57, P=0. 0. 0.0002) reduced the duration of tonic-clonic convulsions in the test animals. It (30 mg kg -1 100 mg kg -1 and 300 mg kg -1 ) also significantly (P=0.0.0004: F3, 24 =8.422) increased the latency fig. 4.4A to the first myoclonic jerk . For the frequency of convulsions, only 100 mg kg -1 reduced the frequency but not significantly (P=0.0779: F3, 16 =2.735); fig 4.4B. The standard control phenobarbitone, reduced the frequency but not significantly (F3, 16=0.0779, P=0. 2.735) and significantly reduced both the duration (P=0.0.0403: F3, 16 =3.491) of picrotoxin-induced convulsions and also increased significantly (P=0.0007: F3, 16 =49.811) the latency to convulsions in the 3, 10, and 30 mg kg -1 groups (Figure 4.4). University of Ghana http://ugspace.ug.edu.gh 47 Figure 4.4:Effect of ECE 30, 100, 300 mg kg-1 and phenobarbitone 3, 10, 30 mg kg-1 on the latencies to first myoclonic jerks, the total frequency of the seizures, and total frequency of the seizures induced by picrotoxin. Each column represents the mean ± SEM (n = 5). *P < 0.05, **P < 0.01compared with vehicle-treated group (one-way analysis of variance followed by Newman–Keuls post hoc test). University of Ghana http://ugspace.ug.edu.gh 48 1.22.3 MAXIMAL ELECTROSHOCK TEST The maximal electroshock model administered electric current (50 Hz, 60 mA, and 0.2 s) which induced hind limb tonic extensions in all animals pre-treated. For Ehretia cymosa, only the highest dose 300 mg kg -1 significantly (P<=0.0167: F3, 16 = 4.151) reduced the duration of the first hind limb tonic extensions (HLTE); fig. 4.5A. The extract also delayed the total duration of the HLTE but was not statistically significant (F3, 16= 0.3300, P=0. 0.8037); fig. 4.6C. The standard drug carbamazepine did not reduce the duration of first hind limb tonic extensions (HLTE) (P=0.0791: F3, 16 =2.554) nor the total duration of the tonic hind limb convulsions (Fig. 4.5B and Fig. 4.6D). University of Ghana http://ugspace.ug.edu.gh 49 Figure 4.5: Effect of ECE 30, 100 and 300 mg kg -1 and carbamazepine 3, 10 and 30 mg kg -1 on the duration of First HLE induced by Maximal Electroshock Test (MEST). Each column represents the mean ± SEM (n = 7). *P < 0.05, **P < 0.01 ***P < 0.001 compared with vehicle-treated group (one-way analysis of variance followed by Newman–Keuls post hoc test). University of Ghana http://ugspace.ug.edu.gh 50 Figure 4.6: Effect of ECE 30, 100 and 300 mg kg -1 and carbamazepine 3, 10 and 30 mg kg -1 on the total duration of Hind Limb Extensions (HLE) induced by Maximal Electroshock Test (MEST). Each column represents the mean ± SEM (n = 5). *P < 0.05, **P < 0.01 ***P < 0.001 compared with vehicle-treated group (one-way analysis of variance followed by Newman–Keuls post hoc test). 1.22.4 PTZ KINDLING TEST The experiment involved giving the vehicle-treated group, a repeated administration of 35 mg kg -1 of PTZ on alternate days which caused a gradual increase in the convulsant‘s responses as scored using the Racine scale. The score had increased from 0 to 3 by the 9 th day and maintained a Racine score of 4 from the 27 th to the 39 th day and reached a peak severity of Racine score of 5 by the 41 st day which was maintained for 2 weeks (Fig. 4.7A). ECE significantly depressed the kindled seizures at all the dose levels tested (F3, 84 = 24.97, P< 0.0001); fig. 4.7B. None of the animals in the extract-treated groups achieved seizure score 5, even after 22 injections of PTZ 35 mg kg -1 . The percentage severity of seizures (calculated from the AUC) shows that ECE attenuated PTZ kindled seizure activity by reducing the severity of seizures by 50%--70%. Phenobarbitone also produced a significant dose-dependent Veh 30 100 300 0 5 10 15 20 (C) ECE (mg/kg) T o ta l D u ra ti o n o f H L E Vehicle 3 10 30 0 5 10 15 20 25 (D) Carbamazepine (mg/kg) T o ta l D u ra ti o n o f H L E University of Ghana http://ugspace.ug.edu.gh 51 depression of the kindled seizure activity (F3, 84 = 38.09, P < 0.0001); fig. 4.7D, and the percent severity of seizures was significantly reduced by 70% (Figure 4.7). University of Ghana http://ugspace.ug.edu.gh 52 Figure 4.7:The dose-response effects of ECE 30, 100, and 300 mg kg -1 (A and B) and phenobarbitone 3, 10, and 30 mg kg -1 (C and D) on the PTZ-kindled mice. The left panels show the time course of effects over the 32 days and the right panels show the percent severity of seizures calculated from the AUCs for the test duration. Values are means ± SEM (n=10). *P < 0.05, ** P < 0.01, ***P < 0.001 compared with vehicle-treated group (two- way analysis of variance followed by Bonferroni’spost hoc test). †P<0.05, †††P<0.001 compared with the vehicle-treated group (one-way analysis of variance followed by Newman–Keul’spost hoc test). University of Ghana http://ugspace.ug.edu.gh 53 1.23 TOXICITY STUDIES 1.23.1 BIOCHEMICAL PARAMETERS The study evaluated the lipid profile, kidney and liver functions of the animals. There was no significant difference (P=0.08-0.99) between the vehicle-treated and the ECE (30, 100, and 300 mg kg -1 )-treated rats regarding the serum concentrations of urea or creatinine (kidney function) of the rat subjects. There was also no significant difference between the treatment groups with regards to HDL (P=0.99), LDL (P=0.92), total cholesterol (P=0.51), and triglycerides (P=0.25), when compared to the control. The other parameters measured for the lipid profile were not significantly different (P=0.25-0.99) for the ECE-treated animals and the vehicle. However, ECE-treated rats (30 mg kg -1 ) showed significant difference in direct bilirubin (P=0.02) when compared to vehicle-treated rats (Table 4.3). University of Ghana http://ugspace.ug.edu.gh 54 Table 4.3: A table showing the biochemical analysis of a single administration of ECE (30, 100 and 300 mg kg -1 ) after a 72-day study period in Sprague-Dawley male rats Parameters Vehicle ECE 30 ECE 100 ECE 300 P-value Renal function test (mmol L -1 ) Urea 8.41 ± 1.46 8.14 ± 0.78 8.34 ± 0.92 8.34 ± 0.36 0.99 Creatinine 67.04± 12.06 38.38 ± 2.37 42.72 ± 6.24 46.66 ± 4.30 0.08 Lipid Profile (mmol L -1 ) Total Cholesterol 2.04 ± 0.10 1.85± 0.14 2.0 ± 0.16 2.25 ± 0.11 0.51 Triglycerides 1.41 ± 0.21 1.30 ± 0.06 1.21 ± 0.28 1.77 ± 0.16 0.25 HDL 0.92 ± 0.11 0.86 ± 0.058 1.13 ± 0.09 1.19 ± 0.11 0.99 LDL 0.48 ± 0.12 0.48 ± 00.11 0.43 ± 0.072 0.51 ± 0.11 0.92 Liver function test Total Protein (g L-1) 88.98± 2.21 81.13±1.713 81.64±4.647 85.46±1.617 0.24 University of Ghana http://ugspace.ug.edu.gh 55 Albumin (gL-1) 39.44± 1.247 35.70±1.369 37.64±2.157 37.56± 0.96 0.44 D.Bilirubin (μmolL-1) 1.33 ± 0.024 1.003±0.059 1.22 ± 0.089 1.23± 0.05 0.02* Ind.Bilirubin (μmolL-1) 0.54 ± 0.44 0.43 ± 0.13 0.52 ± 0.17 1.30±0.1897 0.13 T.Bilirubin (μmolL-1) 1.86 ± 0.44 1.45± 0.15 1.76± 0.20 2.53 ± 0.16 0.09 ALT (UL-1) 91.50 ± 27.92 67.73±5.663 88.76±19.23 87.90±6.624 0.82 AST (IUL-1) 269.6 ± 42.09 183.4±18.09 276.5±55.94 205.5±27.65 0.32 University of Ghana http://ugspace.ug.edu.gh 56 1.23.2 HISTOLOGICAL EXAMINATION OF ISOLATED TISSUES . The liver of extract-treated rats showed normal liver sections with a characteristic hexagonal arrangement of hepatocytes in lobules surrounding a central vein (Figure 4.9). The examination of the heart sections showed a characteristic branching arrangement of myocardial fibres with centrally placed nuclei (Figure 4.11). The kidney sections revealed normal tubules, glomeruli, and renal capsules (Figure 4.10). The histology of the lungs showed normal alveolar sacs, alveoli as well as alveolar ducts, bronchus, and bronchioles. Lastly, the sectioned brain revealed normal pia mater, molecular layer, granular layer, and white matter as well as dura mater and with normal Purkinje and pyramidal cells (Figure 4.8). There were no distortions of the normal architecture of tissues of any of the organs with immigrant cell types which may have constituted a form of pathology in all the doses levels as compared to that of the control. Figure 4.8: The Photomicrographs of Brain isolated from rats after 72-day continuous administration of (A) Vehicle, (B) ECE (30, 100 and 300 mg kg -1 ), (H&E staining, 40×). University of Ghana http://ugspace.ug.edu.gh 57 Figure 4.9:The Photomicrographs of livers isolated from rats after 72-day continuous administration of (A) Vehicle, (B) 30 (C) 100 and (D) 300 mg kg -1 ) (H&E staining, 40×). The arrow shows the evenly distributed hepatocytes. University of Ghana http://ugspace.ug.edu.gh 58 Figure 4.10:Photomicrographs of kidneys isolated from rats after 72-day continuous administration of (A) Vehicle, (B) ECE 30, (C) 100 and (D) 300 mg kg -1 showing normal renal tubule and glomeruli (H&E staining, 40×). University of Ghana http://ugspace.ug.edu.gh 59 Figure 4.11:Photomicrographs of hearts isolated from rats after 72-day continuous administration of (A) Vehicle, (B) 30, (C) 100, (D) ECE 300 mg kg -1 ) showing normal myocardial fibers with characteristic central nuclei and branching arrangement as indicated by the arrows. University of Ghana http://ugspace.ug.edu.gh 60 CHAPTER 5 DISCUSSION The present work demonstrated that ECE has anticonvulsant potential. The extract reduced seizure activity in mice in various models at doses that were considered non-toxic. Animal models used for screening the pharmacological effect of ECE include Irwin‘s test, PTZ- kindling, picrotoxin induced seizure test, rotarod test, maximal electroshock test, the hotplate test and acute and sub-chronic toxicity studies. Irwin observation test is employed to assess the effects of an investigative drug on physiological and behavioural activity. The results obtained from this test are used to assess the potential toxicity and to help in the selection of doses for a particular neuropharmacological investigation (Vogel et al., 2015). It provides an understanding of the possible toxicity or otherwise of the test substance. From this, novel therapeutic agents may be discovered through a systematic way of assessing behavioural and physiological functions of the test substance qualitatively (Biney et al., 2014; Irwin, 1968). After the observation test employing an oral gavage of 6 different doses of the extract and control, mortality was zero after 48 hours and the LD50 was found to be greater than 3000 mg kg -1 . Irwin test revealed reduced sensitivity to tail pinch touch indicating a potential analgesic effect, and reduced activity which also indicated potential sedative and neuromuscular effects. There was however altered respiration and slight tremors elicited at higher doses of 1000 and 3000 mg kg -1 but mortality was zero in these groups too. Most of the CNS effect was elicited at the 30, 100 and 300 mg kg -1 dose groups and no tremors or altered respiration was also seen in those groups. The CNS effects were mostly elicited between University of Ghana http://ugspace.ug.edu.gh 61 30 minutes to one hour after the oral administration. Based on these findings, the 30, 100, and 300 mg kg -1 dose groups were selected for this work, and a one hour waiting time was also selected as pre-treatment time for this work. From Irwin test, a potential neuromuscular effect of the extract was indicated so the rotarod apparatus test was used to validate that effect. The rotarod test is used to assess the behavioural effect of drugs on motor coordination (Vogel et al., 2015). The present study showed that ECE could cause a reduction in time spent on the rotating rod but this was not statistically significant at all doses tested i.e. 30, 100, 300 mg kg -1 . This means that the doses that can cause a potential reduction in neuromuscular activity with regards to the effects seen or elicited during Irwin's test can be said to be above the doses 30, 100, and 300 mg kg -1 that were used for this work. The hot plate test is a simple behavioural test used for assessing the consequence of investigative drugs on the pain threshold sensitivity. The test is based on the logic that rodents will lick their paws or attempt escaping by jumping when they are put on a hot surface,. Investigative drugs that can alter the nociception threshold will either increase the latency to jumping or licking indicating an analgesic effect while those with hyperalgesic effect decrease the latency to licking/jumping (Vogel et al., 2015). The test, however, could not significantly increase the latency (F 3, 8 =2.907 P=0.1011 fig 4.1) as compared to the control. It increased the latency to paw licking of the 100 and 300 mg kg -1 but not significantly when compared to the control. But again, drugs that have a low analgesic effects, specifically, those that are essentially anti-inflammatory agents like ibuprofen, University of Ghana http://ugspace.ug.edu.gh 62 aspirin and paracetamol, exhibit less pronounced outcome than well-known analgesics such as the opioids (Vogel et al., 2015). This means that the extract‘s possible analgesic effect seen during Irwin test could be due to the extract's anti-inflammatory effects and not necessarily an analgesic effect. This experimental work employed various models of seizures and provided evidence that the ethanolic extract of the leaves of Ehretia cymosa has anticonvulsant activity and that the extract is also safe in murine models. The anticonvulsant activity was evident in both the acute and chronic models of seizures and no toxicity was recorded in both models of toxicity that were used. The study employed convulsive threshold tests that are used in estimating the probability of an investigative drug to induce alterations in the propensity to the occurrence of seizures either spontaneously or, more importantly, in the company with other treatments (Vogel et al., 2015). In the acute models, PTZ, picrotoxin, and the maximal electroshock tests were employed whereas the PTZ kindling model was used for the chronic model. The PTZ acute model is a model that is thought to have an antagonistic action on GABAA receptors (Auvin & Nehlig, 2017) and represents a well-founded model for human absence and generalized seizures (Patrick Amoateng, Eric Woode, & Samuel B Kombian, 2012; Löscher & Schmidt, 1988). The extract elicited anticonvulsant activity against seizures induced by PTZ by increasing the latency to the first myoclonic jerks and clonic seizures in mice as well as reducingthe duration and frequency of the clonic seizures. Thus, the ability of the extract to inhibit seizures induc