Anti-epileptic drugs (AED) and their interactions with CNS anti-neoplastic drugs
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He graduated and obtained his Ph.D. in Applied Life Sciences from Tokyo University of Agriculture and Technology (Japan) in 2011. He was awarded Japanese government scholarship and he visited University of California at Davis (UCD) as an exchange student in 2010. After his graduation, he became a research fellow at the German Cancer Research Center (Deutsches Krebsforschungszentrum, DKFZ) in Heidelberg (Germany). Dr. Ying acts as a reviewer of many scientific journals and has authored or co-authored over 25 scientific publications. His research interests include molecular mechanisms of post-translational modification, such as SUMOylation, citrullination, and their clinical relevance in human diseases.",institutionString:"Hangzhou Medical College",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"1",totalChapterViews:"0",totalEditedBooks:"0",institution:null}],coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"6",title:"Biochemistry, Genetics and Molecular Biology",slug:"biochemistry-genetics-and-molecular-biology"}],chapters:null,productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},personalPublishingAssistant:{id:"259492",firstName:"Sara",lastName:"Gojević-Zrnić",middleName:null,title:"Mrs.",imageUrl:"https://mts.intechopen.com/storage/users/259492/images/7469_n.png",email:"sara.p@intechopen.com",biography:"As an Author Service Manager my responsibilities include monitoring and facilitating all publishing activities for authors and editors. 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Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"878",title:"Phytochemicals",subtitle:"A Global Perspective of Their Role in Nutrition and Health",isOpenForSubmission:!1,hash:"ec77671f63975ef2d16192897deb6835",slug:"phytochemicals-a-global-perspective-of-their-role-in-nutrition-and-health",bookSignature:"Venketeshwer Rao",coverURL:"https://cdn.intechopen.com/books/images_new/878.jpg",editedByType:"Edited by",editors:[{id:"82663",title:"Dr.",name:"Venketeshwer",surname:"Rao",slug:"venketeshwer-rao",fullName:"Venketeshwer Rao"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"4816",title:"Face Recognition",subtitle:null,isOpenForSubmission:!1,hash:"146063b5359146b7718ea86bad47c8eb",slug:"face_recognition",bookSignature:"Kresimir Delac and Mislav Grgic",coverURL:"https://cdn.intechopen.com/books/images_new/4816.jpg",editedByType:"Edited by",editors:[{id:"528",title:"Dr.",name:"Kresimir",surname:"Delac",slug:"kresimir-delac",fullName:"Kresimir Delac"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"47677",title:"Seizures in Children with Brain Tumours — Epidemiology, Significance, Management, and Outcomes",doi:"10.5772/58961",slug:"seizures-in-children-with-brain-tumours-epidemiology-significance-management-and-outcomes",body:'Cancer is the most frequently diagnosed disease-related cause of death among children and adolescents [1], and malignancies involving the brain are collectively the most common solid tumour [2, 3]. They are also either first or second in incidence overall (second only to leukaemia) in the United States (USA) [1, 4,7], Canada [8], and Mexico [9]. The American Brain Tumour Association has estimated that approximately 4,200 American children younger than age 20 would be diagnosed with a primary brain tumour in the year 2012, of whom three in four would be under the age of 15 years [10]. However, the overall prognosis for brain malignancies is much better in children than in adults, with up to half of paediatric brain cancer patients surviving long-term [11]. The reason for this enhanced survival in youths is that children and adolescents are much more likely than adults to have low-grade astrocytomas, in particular pilocytic astrocytomas and other low-grade gliomas that are almost never fatal and often cured, depending upon their location and surgical accessibility, rather than the grade III and IV astrocytomas that account for the majority of tumours among adults [12-14].
Long-term survival, even in the setting of cure, is not without problems, however, with empirical evidence accumulating that paediatric brain cancer survivors continue to suffer from significant morbidity [15-20] and, sometimes, early death [15]. Among the more common long-term sequelae of brain cancer and brain cancer treatment in children are seizures, which can be quite disabling and, at times, life-threatening in themselves [15, 21-30]. In one study, seizures were the number one predictor of disability in long-term brain cancer survivors [24, 25]. Seizures even increase a paediatric survivor’s risk of suicide into adulthood [31]. In addition, there is a subset of children, up to 50% [32], whose low-grade brain cancer presents as seizures [26, 32-42]. Though the vast majority of epileptogenic tumours are supratentorial, some are not, especially among children in whom infratentorial tumours generally comprise the majority [43, 44], and in less typical locations like the thalamus and hypothalamus [38, 45-47]. Among thalamic tumours, for example, up to one third of paediatric patients present with seizures [38]. As such, and because even low-grade gliomas can nonetheless be infiltrative into high-function brain tissue [19, 48-50], while some of these lesions are totally resectable, others are not [51-54]. This creates dilemmas as to how aggressive to be, and therefore how much risk to take in their resection [55]. As well, the return of seizures at some distant time post-operatively may indicate tumour growth or relapse [28, 30, 56-66], transformation into a more aggressive lesion [28, 60, 65, 67, 68], or even the emergence of a secondary (e.g., radiation-induced) tumour [64].
Why seizures occur in patients with brain tumours is not entirely clear [27, 69-71], and several conjectures have been made, including alterations in regional metabolism and pH, immunologic activity, disordered neuronal function, altered vascular supply and permeability, the release of altered tumoral amino acids, proteins and enzymes, and abnormal protein transport and binding to receptors [27, 44, 69, 71-74]. Even genetic predispositions for tumour-related seizures have been postulated [71, 75]. A recent excellent review of current theories and empirical evidence on the pathogenesis of tumour-related epilepsy has been published by You et al. [74] Discussing the relative merits of each theory is a paper in itself, and beyond the scope of the current review.
Interestingly, tumour size has a somewhat paradoxical relationship with seizure occurrence, in that, though the opposite is true of low-grade lesions, high-grade gliomas that present with seizures tend to be smaller than those that present with other symptoms [76]. Moreover, high-grade lesions that present with seizures tend to have a better prognosis than lesions of the same size that present otherwise [77]. What this suggests is that the aggressiveness of the tumour might have an effect upon seizure development. This being said, low-grade lesions comprise the majority of epileptogenic tumours, both in children and adults [78]; and some tumour types — like gangliogliomas and dysembryoplastic neuroepithelial tumours (DNET) — are more likely to induce seizures than others [28].
In this chapter, we will thoroughly review the literature on seizures in paediatric brain cancer patients, looking at them (1) as a presenting symptom; (2) in the early tumour management/peri-operative period; and (3) long-term. Specific questions to be addressed in each of these sections are: How common are they? What is their history? How do they impact patients’ lives, both short-and long-term, and in terms of management and prognosis? How do they effect management of the underlying tumour? How are seizures managed themselves? As much as possible, these questions will be answered by examining empirical evidence across a number of studies to provide, if not definitive answers, at least conclusions that are supported by published research.
A brain tumour is ultimately discovered in between one and three percent of children who present with new-onset seizures [40, 42], though a slightly higher percentage has been reported in children presenting with partial versus generalized seizures [79], and percentages as high as 20% have been reported in children undergoing epilepsy surgery [80]. From the reverse perspective, somewhere between 10 and 50% of brain tumours present with seizures as a symptom [69, 74, 81-83], and sometimes as the only symptom [32, 41, 84-86], with supratentorial and especially temporal lesions the most likely to be epileptogenic [44, 66, 78, 86-88]. In one study that compared children with supra-and infratentorial tumours, for example, among those with supratentorial lesions, 42% experienced vomiting as their first symptom, followed by seizures in 37%, and headache in 31% [43]. Meanwhile, 62% of children with an infratentorial lesion experienced headaches as their first symptom, with vomiting and ataxia accounting for most of the remainder, and seizures not observed in a single case.
Because children are more likely than adults to have infra-versus supratentorial lesions, the percentage of children presenting with seizures may be somewhat less than among adults, closer to the 10-20% than the 30-50% range [51, 89, 90], though 50% or more has been reported in some series [32, 35]. As in adults, of these epileptic tumours, the vast majority are supratentorial. For example, in their series of 157 children presenting to the hospital with brain tumour-related seizures, of mean age 3.3 years, Khan et al. found that 81% of the tumours were supratentorial and just 19% within the posterior fossa [82]. Meanwhile, Ianelli et al. reported that 80% of their 37 paediatric patients presenting with a temporal lobe malignancy had seizures as a presenting symptom [86]. Another excellent study on new-onset seizures presenting in children with brain cancers was published by Shady et al. [32] who analyzed 98 paediatric brain tumour patients and found that 50% percent of the children had seizures as part of their presentation, and 30% as their only presenting phenomenon; complex (55%) and simple (28%) partial seizures were the most common types, accounting for more than three quarters of all cases. Pre-operative electroencephalography (EEG) accurately lateralized to the tumour side in 88% of the cases and to the correct lobe in 56%. In addition, tumours involving cerebral cortex were much more likely than non-cortical lesions to present with seizures (59% vs. 15% of patients, respectively), with temporal and frontal lobe lesions exhibiting the highest incidence of seizures. Moreover, whereas 88% of gangliogliomas and 86% of oligoastrocytomas were associated with seizures, seizures were noted in just 21% of the patients with an anaplastic astrocytoma. Finally, as described elsewhere [32, 77], patients with seizures at presentation had a better prognosis than those without (p=0.02) [32].
Virtually every possible tumour type has been reported presenting as seizures, especially low-grade gliomas [27, 30, 32, 34, 37, 39, 70-72, 75, 76, 78, 91-93] and glioneuronal tumours like ganglioglioma and dysembryoplastic neuroepithelial tumour [28, 44, 62, 73, 88, 89, 91, 94, 95]; but including oligodendroglioma [77, 96, 97], cortical ependymoma [98], medulloblastoma [47], subependymal giant cell astrocytoma (SEGA) [99], meningioma [10]0, thalamic and cerebellar glioma [38, 46], and a variety of atypical, systemic and metastatic tumours, like primary meningeal osteosarcoma [84], acute lymphoblastic leukemia [101], anaplastic large cell lymphoma [102], neuroblastoma [103], melanoma [104], various sarcomas [105, 106], Ewing’s sarcoma [107], malignant germ cell tumours [108], and others [16, 109].
There is no stereotypical seizure presenting as an early symptom of a brain tumour. Early seizures may be generalized, simple partial, complex partial, or mixed, depending upon the tumour’s size, location, level of aggressiveness, and other factors [24, 26, 27, 33, 34, 37, 70, 74, 77, 82, 87, 110-115]. This being said, among children, seizures as a presenting symptom of brain tumour are most commonly complex or simple partial, versus generalized, with complex partial seizures generally accounting for from 50% to as high as 85% of all new-onset seizures [32, 63, 69, 86, 115-117]. The lone series in which this was not true was that reported by Hirsch et al., in which complex and simple partial seizures together only accounted for half of all cases [118]. The percentages generally reported for children and adolescents are somewhat different than for adults, in whom tumour-associated seizures tend to be more evenly distributed across the four most typical seizure types [58]. Other atypical and, therefore, less well recognized forms of seizure have been described in children as well, including gelastic seizures, characterized by uncontrolled fits of inappropriate laughter [45], tics and Tourrette-like symptoms [119], and sympathetic storms in a 7-year old with a midbrain glioma [120]. In addition, especially in the paediatric population, tumors may arise in the setting of a variety of familial syndromes such as neurofibromatosis types 1 [121] and 2 [122], and tuberous sclerosis [123]. Seizures in these conditions are often blong-standing, frequent, and intractable because of the numerous non-neoplastic lesions that can involve the CNS [55, 124, 125]. In such patients, the diagnosis of a new neoplastic lesion can be especially challenging [124, 126].
The diagnosis of brain tumour does not always quickly follow the onset of seizures. In one study reported by Ibrahim et al., for example, the time from seizure onset to tumour diagnosis among ten children presenting with seizures ranged from two weeks to two years, averaging six months [37]. A wide range of opinions and practices exist regarding how aggressive to pursue diagnostic imaging in children presenting with seizures [36, 41, 51, 79, 80, 100, 127-133]. For example, in one series of eighteen patients between the ages of 1 month and 13 years who presented with seizures and were discovered to have DNETs between January 1992 and December 2004, the preoperative evaluation included magnetic resonance (MR) imaging and interictal scalp electro-encephalography (EEG) in all patients, but functional MR imaging also was performed in eight patients, video monitoring with scalp EEG during seizures in 12 patients, interictal single-photon emission computerized tomography (SPECT) scanning in one patient, and ictal SPECT scanning in two patients [132]. Meanwhile, in their 2010 review of eleven clinical trials for anti-epileptic drugs (AEDs) conducted over the preceding two years, Jansky et al. noted that none of the trials required MRI as part of the patient enrollment protocol [128]. Increasingly, with advances in imaging and the recognition that the resection of epileptogenic lesions is both safe and effective for many patients, there seems to be growing opinion that the initial work-up of new-onset non-febrile seizures in children should include both an EEG and MRI, despite the likelihood that the majority of imaging studies will be either normal or inconclusive [134, 135]. As discussed in the next section, mounting evidence suggests that new-onset seizures in the setting of a tumour, and conversely, tumours in the setting of new-onset seizures both have therapeutic and prognostic implications.
Having a child’s brain tumour present as seizures adds therapeutic complexity with respect to how the patient is initially managed, since peri-operative control of seizures is obviously considered of extreme clinical importance. The type of seizure a patient has also may have prognostic significance, both in terms of patient survival [65, 136] and how easily the seizures are controlled with anti-epilepsy drugs (AED), both peri-operatively and long-term. How well AEDs work, in turn, may have implications relating to how aggressive surgical resection should be.
Although no reliable data have been published for children, adults who present with seizures as their sole symptom tend to have less aggressive or advanced lesions than those who present with symptoms or signs of increased intracranial pressure like papilloedema, headaches [65], neurological or cognitive deficits [65, 136]. Although this intrinsically makes sense — the fewer the symptoms, the less aggressive or advanced the disease — extrapolating these findings to children must be done with caution, because a disproportionate number of paediatric lesions tend to be brainstem tumours that, though usually low-grade and non-epileptogenic, often are non-resectable because of their location and proximity to function-rich neural tissue [2, 3, 137-139]. Nonetheless, especially among supratentorial lesions, it makes sense that having seizures present before all other symptoms develop is a hopeful prognostic sign, given that low-grade gliomas and other so-called benign lesions tend to be associated with much higher seizure rates than high-grade lesions [32, 87, 91, 113, 140, 141].
Having seizures in the presence of a tumour has implications with respect to management of the seizures as well, in that studies have shown that such seizures tend to be more resistant to AEDs than idiopathic seizures [133, 142]. This appears to be especially true for patients who present with a history of numerous seizures [142]. This likelihood of drug resistance, which has been formally defined as “the failure of adequate trials of two tolerated, appropriately-chosen and used antiepileptic drug schedules (whether as monotherapies or in combination) to achieve sustained seizure freedom” [143], may play a role in determining the aggressiveness of surgery for tumour resection. For example, given the clear superiority of epilepsy surgery over medical management alone, in terms of achieving freedom from seizures in patients with intractable seizures (65% vs. 8% in one relatively recent meta-analysis [144]), a decision might be made to pursue more aggressive resection in a patient with repeated new-onset seizures upon initial work-up of seizures and diagnosis of their brain tumour, versus the patient who presents with a single seizure prior to tumour detection. Moreover, for many epileptogenic lesions, surgical resection often leads to either complete resolution of seizures, sometimes without the need for continued AEDs, or to a marked reduction in their frequency, as will be elaborated upon next.
How tumor-induced seizures are managed largely depends upon the aggressiveness and location, and therefore, the prognosis of the underlying tumour. In patients with invariably terminal forms of cancer, including primary brain neoplasms like glioblastoma multiforme (GBM), and metastatic spread to brain, the goal usually is to prolong life over months to, at most, a few years, while preserving as high a quality of life as possible. In both adult and paediatric patients with high-grade astrocytomas like GBM, even partial resection of terminal lesions has been shown both to prolong life and reduce the frequency and severity of seizures [145-147]. Clearly, such surgery needs to be performed as soon after diagnosis of the lesion as possible to have any effect upon outcome. Such is not the case in many patients with low-grade tumours like stage I and II gliomas and gangliogliomas, in whom progression of the tumour may be so slow as to be virtually undetectable, and patients can live for years without apparent disease progression, so that any decision to surgically remove the offending lesion may be delayed for years [58, 93, 148, 149]. This being said, there has been increasing emphasis on surgically resecting low-grade tumours early in the course of disease [131] for a multiplicity of reasons. Among these reasons are that anywhere from 20% to roughly one third of low-grade gliomas (LGG) fail to respond to anti-epileptic medications [72, 150], and many that do respond require more than a single AED [150], placing patients, and especially children, at risk for long-term drug toxicities [23, 24, 59, 71, 151-153]. Among the various documented toxicities of AEDs are wide-ranging adverse effects on cognitive function [23, 153], which already may be impaired because of the tumour itself and the radiation therapy sometimes administered to treat it [18, 20, 154-156]. Moreover, surgical resection of LGG has been shown to enhance long-term survival [19] and to significantly improve the likelihood of seizure control [27, 70].
Though the data are not definitive, there is some evidence suggesting that, among the various seizure types, partial seizures, either simple or complex, may be less likely to respond to anti-epileptic drugs than generalized or mixed seizures [93, 157, 158]. This resistance may be noted initially, so that seizure control is never achieved; but it also may develop over time, so that seizure control is lost and never regained [158, 159]. In such patients, therefore, there may even be an increased incentive to pursue surgical resection of the tumour+/-any adjacent epileptogenic foci, if the lesion can be accessed with no undue risk.
Several studies have shown that radical removal of an epileptogenic brain tumour is a strong, and likely the strongest, predictor of seizure freedom [127]. However, additional predictors include the type of seizure, the histopathology of the tumour, the age of the patient at the time of surgery, and the duration of epilepsy [127]. Among the various tumour histologies, tumours that are non-resectable due to infiltration, like high-grade astrocytomas, can be problematic over the patient’s relatively brief period of survival [160]. However, as stated earlier, such high-grade lesions tend to be less often epileptogenic than their low-grade counterparts [32, 87, 91, 113, 140, 141]. In long-term brain cancer survivors, glioneuronal tumours, and particularly low-grade gliomas, gangliogliomas and dysembryoplastic neuroepithelial tumours (DNETs), often produce quite drug-resistant epilepsy in children, so that complete surgical resection of the tumour is typically considered the primary focus of treatment [28, 61-63, 88, 94, 116, 132]. In such patients, post-operative seizure-freedom rates often approach or exceed 80% [35, 48, 51, 58, 66, 86, 88, 90, 93, 115, 157, 161-169].
Traditionally, there has been some concern about being too aggressive with younger children with brain tumours, because of the risk of long-term adverse effects on neurological development, the risk of secondary neoplasms, and other neurological sequelae [155]. That such risks exist is certainly true of radiation therapy [18, 20, 64, 153-156], but it also is true of surgery [170]. However, recent studies have shown that surgery to resect epileptogenic brain tumours is both effective and safe for the vast majority of infants and toddlers [35, 55, 171]. In one large survey, for example, data were collected retrospectively on 116 patients less than 3-years old from eight centers across Canada from January 1987 to September 2005 who had undergone epilepsy surgery [171]. Among the various seizure aetiologies were malformations of cortical development (n=57), tumours (22), Sturge-Weber syndrome (19), and infarcts (8), with 10 cases either of unknown or some other cause. Seizure onset was in the first year of life in 82%, and the mean age at the time of the initial surgery was 15.8 months (range: 1-35 months). Second surgeries were performed in 27 patients, with six patients requiring a third surgical procedure. Among the initial 116 procedures performed were 40 hemispheric operations, 33 cortical resections, 35 lesionectomies, 7 temporal lobectomies, and one callosotomy. Of the 151 operations, including the 27 second and six third procedures, only one resulted in a surgery-related death. The most common surgical complications were infection, in 17 patients, and aseptic meningitis in 13. Of 107 patients assessed more than one year postoperatively, 72 (67.3%) were seizure free (Engel I), 15(14%) had experienced at least a 90% reduction in seizures (Engel II), and 12 had at least a 50% reduction (Engel III), with only eight exhibiting no benefit (Engel IV). Moreover, 55.3% of the children exhibited signs of improved development post-operatively [171].
Consequently, regardless of patient age, the focus for most patients with low-grade lesions has become, whenever possible without the undue risk of peri-operative death or long-term adverse neurological sequelae, to attempt total or at least subtotal tumor resection earlier rather than later in the course of disease. Debate rages, however, as to how aggressive to be achieving this goal, whether or not resecting the lesion alone is enough, and what intra-operative technologies to use to aid in identifying tumour margins and other epileptogenic foci. Moreover, not all patients will be eligible for surgery and will have to rely on non-neurosurgical treatments alone, most notably anti-epileptic drugs (AEDs) and radiation therapy. The next section briefly discusses the benefits, risks and utilization of AEDs both prior to and in lieu of surgery.
An extensive review paper could be written discussing the various advantages and disadvantages, indications and contra-indications, and drug-drug interactions that exist for the extensive list of anti-epileptic drugs that now are available for use in patients with brain tumour-induced epilepsy, all of which is beyond the scope of the current review. Here, we briefly describe the roles of AEDs, both in prophylaxis against and control of tumour-induced seizures, some of the risks of prolonged use, and at least the theoretical advantages of the new class of non-enzyme inducing drugs.
In three recent surveys of neurosurgeons, including one survey specifically of members of the American Association of Neurologic Surgeons (AANS), the majority (up to 70%) of respondents reported prophylactically initiating AEDs in brain tumour patients who had not yet experienced a seizure [172-174]. This practice of prescribing AEDs prophylactically in brain tumour patients with no seizure history persists, even though empirical evidence addressing this practice is inconclusive at best [78, 81, 127, 140, 172]. Moreover, many authors and the most current American Association of Neurology practice parameters argue against it [113, 140, 172, 175, 176]. The argument of AED detractors is that both meta-analyses published since 2000 to address this issue failed to provide sufficient evidence to promote their prophylactic use in brain-tumour patients without seizures [173, 177]. The first meta-analysis, published in 2000 by Glantz et al. [173], analyzed 12 studies, of which four were randomized controlled trials and eight were considered to be “well-designed observational studies with concurrent controls”, sufficient to be classified as class II evidence. Not one of these twelve studies demonstrated a statistical advantage of the AED being studied (phenytoin, depakote, or phenobarbital) over placebo [173]. The second, somewhat more stringent meta-analysis, published in 2004 by Sirven et al [177], only included five RCTs, assessing the prophylactic use of either phenobarbital, phenytoin, or valproic acid. Of the five trials, four identified no statistical benefit of AED use for peri-operative seizure prophylaxis. The one exception was a 1983 study published by North et al [178], in which not only patients with brain tumours, but patients who had undergone craniotomies for aneurisms and head injuries were included. A closer, empirical look at these data reveals no advantage at all when brain tumours are considered alone: seizures occurred in 9/42 on phenytoin, and in 5/39 on placebo (OR=1.11, 95% CI=0.58, 2.12). Further considering just those patients with glial tumours (versus meningiomas, sellar tumours, and metastases), seizures occurred in three of 16 on phenytoin versus just one of 16 on placebo (1.15; 0.42, 3.19) [178]. Overall meta-analysis across the five RCT confirmed the lack of any AED benefit at both one week (OR, 0.91; 95% confidence interval [CI], 0.45-1.83) and six months (OR, 1.01; 95% CI, 0.51-1.98) of follow-up. The AEDs also exhibited no effect on seizure prevention for specific tumours, including primary glial tumors (OR, 3.46; 95% CI, 0.32-37.47), cerebral metastases (OR, 2.50; 95% CI, 0.25-24.72), and meningiomas (OR, 0.62; 95% CI, 0.10-3.85) [177].
More recently, in a review published in 2011, Kargiotis et al. non-statistically examined published evidence on more currently-used AED, including the newer non-enzyme inducing drugs, and concluded that, among patients with either brain metastases or primary brain tumors who have never experienced seizures, prophylactic anticonvulsant treatment might be justified, but only for up to six months postoperatively after surgical excision of the cerebral tumour, since most of these patients will never experience seizures, and the anti-epileptic drugs may cause toxicity and adverse interactions with chemotherapeutic treatments administered to control the neoplasm itself [109]. For such prophylaxis, the authors argued that newer antiepileptic drugs like levetiracetam and oxcarbazepine are preferable to older agents like phenytoin and carbamazepine [109]. To date, however, no hard evidence supports any of these recommendations, and certainly not in children.
In a study by Hardesty et al., only 7.4% of 223 paediatric patients with brain tumours but no history of seizures experienced even a single seizure during their surgical admission, even though only 4.4% of patients had been started on a prophylactic AED [179]. This percentage is similar to the 8.0% observed among those on placebo in a controlled study in which 127 patients awaiting brain tumour surgery, ranging in age from 16 to 84 years, were randomized to receive either phenytoin 15mg/kg intravenously in the operating room, followed by 100 mg three times daily, either by mouth or intravenously, for seven days or placebo [180]. Thereafter, the dose of each was tapered. The 30-day incidence of seizures actually was higher in the phenytoin group (10.0%) than in controls (8.0%), albeit not statistically so. Moreover, the rate of complications was 18.0% versus 0% in the treatment versus placebo group, respectively (p < 0.001).
In the Hardesty study on youths [179], dependent factors associated with peri-operative seizures included a supratentorial tumour, patient age less than two years, and the presence of post-operative hyponatraemia due to either the syndrome of inappropriate antidiuretic hormone (SIADH) or cerebral salt wasting. No other factor was independently predictive of incident seizures, including tumour type, the lobe of the brain affected, the amount of operative blood loss, and the length of surgery [179]. Consequently, though children and adolescents who are awaiting brain-tumour resection and have recurrent seizures might warrant the initiation of an AED pre-operatively, and perhaps also children under age two years with a supratentorial tumour and those with highly-epileptogenic tumours like DNETs, even in the absence of seizures, the prophylactic use of these drugs is far from empirically justified. What is more prudent is to monitor all patients carefully throughout the peri-operative period to identify clinical factors that might place the child at risk, like electrolyte imbalances and fever.
Although in some small series of patients, seizures have been found to occur in up to 50% of paediatric patients with a brain tumour [170], in most populations, the overall incidence of seizures in this patient population is considerably lower, in the 10-20% range [51, 89, 90]. This is largely due to the infratentorial location of the majority of paediatric tumours, where very few are epileptogenic [37]. As such, only a small minority of children and adolescents with a brain tumour will likely ever require an AED, and almost all will have a supratentorial lesion. For example, from a database of 334 patients up to 21-years old, Sogawa et al. only identified 32 (10%) who had been started on an AED [83]; 94% of these 32 tumours were supratentorial, and 78% were glial [83]. Similarly, in their series of 280 patients between the ages of two months and 18 years of age, Khan et al. identified only 55 (20%) patients who had required an AED, among whom 49 (89%) had a supratentorial lesion [90]. This being said, over a 20-year period at a single institution, Khan et al. followed 157 patients who had presented with seizures and a brain tumour during childhood or adolescence, all of whom had been on at least one AED at some point [82]. Of these patients, phenytoin was the first AED used for 52 patients, carbamazepine for 38 patients, gabapentin for 31, and phenobarbitol for 14. Sixty-two of these patients ultimately were taken off all AEDs; but 17 of these 62 (27%) suffered seizure recurrence [181].
DNETs and gangliogliomas, which typically become manifest during childhood, adolescence or young adulthood, represent only a small percentage of CNS tumours in either youths or adults [6]. However, these tumours are almost always associated with seizures. Consequently, they comprise a disproportionate percentage of tumour-associated epilepsy cases [28, 44, 62, 73, 88, 89, 91, 94, 95]. Moreover, DNETs tend to be extremely resistant to AED therapy [62, 182-186]. Consequently, though AEDs generally are initiated in such patients, the majority ultimately will require surgical resection.
There is virtually no debate that AEDs are of use in treating brain tumour patients with seizures, in patients with repeated seizures awaiting surgery, in patients in whom tumour resection is infeasible, and in those whose seizures remain refractory despite surgery. However, there is concern about the risks of their long-term use, especially in patients who require on-going chemotherapy for their brain malignancy due to drug interactions and mutually-shared toxicities [81, 83, 127, 140, 151, 159, 172, 176], 187]; and significant debate regarding when and how AEDs should be discontinued post-operatively.
One of the biggest issues relating to AEDs is their potential interactions with anti-neoplastic drugs administered to control tumours and prolong survival. In a paper reviewing anti-epileptic drugs, Kargiotis et al. [109] listed 25 chemotherapeutic medications that interact with AEDs, most commonly carbamazepine, phenobarbitol, phenytoin and primidone, but also valproic acid. Common interactions are the AED accelerating metabolism of the chemotherapeutic drug, and the chemotherapeutic drug reducing serum levels of the AED [109], two results that potentially accentuate each other — when AED levels fall, AED doses must be increased to achieve seizure control, which will further increase metabolism of the chemotherapeutic drug, resulting in its doses needing to be increased, and so on. Included on their list of 25 drugs were 13 drugs often selected for the treatment of brain metastases, as well as nine drugs currently used to treat glioblastomas, six drugs to treat medulloblastomas, and five to treat malignant meningiomas.
In the current paper, Table 1 lists these interactions in reverse, indicating those anti-neoplastic drugs used for CNS malignancies that have had documented interactions with each of the five AEDs listed above. What is clear from this table is that all but valproic acid interacts with almost all of the chemo-therapeutic drugs typically used for CNS cancers.
The only drug on the list published by Kargiotis et al. [109] this is not considered to interact with AEDs is temozolomide (TMZ), a less toxic and more-easily tolerated orally-administered drug that effectively crosses the blood-brain barrier [188] and is now commonly used for both high-grade [189] and low-grade [190, 191] gliomas, as well as for brain metastases [192] and melanomas, often in combination with radiation therapy. There also is evidence that TMZ itself reduces the frequency of seizures, independent of AED dose. In one study in which 39 patients receiving TMZ (mean age 46.0 years) were followed for a mean 39 months and compared with 30 patients not on TMZ (mean age 41.5 years), patients on TMZ experienced a 59% reduction in seizure frequency versus just 13% in controls (p < 0.001) [150]. However, for reasons that are not entirely understood, TMZ appears to be less effective in children [193]. For this reason, other anti-neoplastic drugs typically are prescribed in children and adolescents, particularly multiple-drug regimens that include carboplatin and vincristine [193-195], two drugs both documented to interact with the older, cytochrome P450-inducing anti-eptileptics [109] (Table 1).
Meanwhile, evidence continues to mount documenting both the effectiveness and safety of newer-generation AEDS, like levetiracetam, oxcarbazepine and pregabalin [152, 196-204]. Though direct comparisons against the older drugs are generally lacking, theoretical advantages include the lack of any effect on cytochrome P450, and the fact that these drugs generally target specific risk factors for tumour-induced seizures [81]. Recently, in a survey of 32 paediatric brain-tumour patients requiring AEDs for seizure control, Sogawa et al. found that patients who had been started on any the newer–generation drugs (levetiracetam, oxcarbazepine and lamotrigine) were three times as likely to remain on these drugs than those started on one of the older drugs like valproic acid, phenytoin, and phenobarbitol (73% vs. 28%, respectively, p=0.04) [83]. Although the sample was small, there also was evidence of increased toxicity with the older drugs, with five versus just two adverse events resulting in drug discontinuation [83].
Of course, the treatment of brain tumours is anything but a static field. In attempts to reduce tumour progression and prolong survival, newer chemotherapeutic drugs are continuously being tested. Some, like nimotuzumab [205]and bevacizumab [206], both of them antibodies against epithelial growth factor receptors (EGFR), have been demonstrating considerable promise, and this may have implications for which AEDs are best tolerated as interactions and mutual toxicities become clearer. What is evident is that AEDs, in themselves, are usually inadequate to control seizures in most patients with epileptogenic brain tumours. And while novel treatments like stereotactic radiosurgery [154], vagus nerve stimulation [207], and ionizing radiation [208] are emerging, at this time optimal management of a child or adolescent with epilepsy caused by a brain tumour almost always necessitates resection of the lesion itself.
In recent years, there has been a trend towards earlier surgical intervention in young patients with low-grade epileptogenic tumours; but is this justified? One potential justification is the risk of malignant transformation of low-grade tumours which, even though uncommon, has been described for virtually all tumour types and often is catastrophic [60, 64, 65, 67, 68, 97, 112, 131, 209-213]. A second justification pertains to improved seizure control and the decreased reliance on AEDs, with some patients potentially able to discontinue anti-epileptic medications altogether59, [61, 181, 185]. But how successful is tumour resection in terms of controlling or eliminating seizures?
Table 2 lists 26 studies [35, 51, [61-63, 86, 90, 94, 96, 132, 148, 149, 168, 182, 184, 185, 214-223] published over the past two decades in which seizure outcomes in children and adolescents undergoing surgery to remove epileptogenic brain neoplasms were examined. Across these 26 studies are 741 patients, ranging in age from one month to 21 years of age, with a mean age of 9.1 years and a mean duration of post-operative follow-up of more than four years (overall mean=52 months, with individual study means ranging from 12 to 148 months). Though one study [86] included six paediatric patients with high-grade gliomas (either GBM or grade III astrocytoma), and another indicated 11 patients with either grade III or grade IV lesions [35], almost all of the remaining 724 patients had low-grade (grade I or II) lesions, including various low-grade gliomas and glioneuronal tumours, and less typically epileptogenic tumours like craniopharyngiomas and a dysplastic cyst. Spanning these studies, surgical approaches clearly differed, with some surgeons either largely or exclusively performing lesionectomies alone, others performing further procedures like partial lobectomies [86, 148] and amygdylohypocampectomies [182], and still others using various intra-operative mapping technologies like electrocortography (ECoG) [63, 132, 184, 214] to identify and ultimately resect extra-tumoral epileptogenic tissue. However, the ubiquitous goal was total tumour resection, whenever possible, an objective that was achieved in roughly two-thirds of cases.
Overall, the series with the lowest total resection rates were those that included a number of oligodendrogliomas (ODG), with resection rates ranging from 30% in a study exclusively of ODG and ODG-mixed lesions [96] and 40% in an older study in which half the patients had ODG [219], to 58% and 61% in studies in which the proportion of ODG was considerably lower [90, 220]. This discovery is not unexpected, given the highly infiltrative nature of these tumours [77, 96, 97, 191].
The outcomes of surgery otherwise were impressive, with almost four out of every five patients (77.7%) seizure free at the time of the final follow-up assessment, and 92.6% experiencing a significant improvement in their seizures from baseline, to Engel class 1, 2 or 3. Examining these data further reveals moderately strong, borderline statistically-significant correlations between the percentage of total resections achieved within any given series and the rate of seizure freedom (r=0.37, p=0.08), and between the percentage of total resections and the percentage of patients whose seizures were improved post-operatively (r=0.36, p=0.09). However, no correlation is apparent between the duration of follow-up and either outcome (r=0.06, p=0.78 and r=0.26, p=0.22, respectively), suggesting that it was the surgical procedure, rather than post-operative management, that influenced seizure outcomes.
There also were no peri-operative deaths among the 741 patients, some of whom even underwent second procedures to resect residual tumour detected by imaging after the first procedure. The overall operative complication rate, adjusted for missing data, was 11.7%, with the vast majority of complications and new neurological deficits transient and completely resolved within weeks to months of the procedure. As stated above, a small number of patients required repeat surgeries to achieve seizure control, sometimes associated with total tumour resection. For example, in one series a second surgery was required in three of 29 paediatric patients with supratentorial gangliogliomas, and all became seizure free after the second operation [216].
The studies by Jo et al. [223] and Gaggero et al. [35] are of special note because all the patients were infants, under the age of 5 and 3 years, respectively. In the first small series of 14 patients of mean age 2.7 years (32 months) [223], total resection of the epileptogenic lesion was achieved in 71%, as was total seizure freedom an average of 35 months post-operatively. In addition, all 14 infants experienced a significant reduction in seizure frequency, either being totally seizure free or having seizures limited to auras alone [223]. There also were no deaths and no reported operative complications. In the second study, which included 20 infants under age 3 years (mean age 1.5 years), eleven of the 20 children had either a grade III or grade IV neoplasm, including four choroid plexus carcinomas, one anaplastic oligodendroglioma, one anaplastic ependymoma, one immature teratoma, two glioblastoma multiforme, one PNET and one neuroblastoma [35]. Despite this, total resection was achieved in 70% of the children, seizure freedom beyond four years in 55%, and seizure improvement in 90%. Interestingly, all 20 patients lived beyond four years, and 17 remained alive at eight years of follow-up [35]. These two studies that imply both the effectiveness and safety of aggressive brain tumour resection in infants is counter to another study on 18 infants under one year of age who had a variety of grade I through IV lesions [170]. In this series, there was only one peri-operative death, due to massive brain haemorrhage in an 8-month old child with a deep, right parieto-occipital ganglioglioma. However, three patients had new-onset seizures following surgery, and an additional three had worsened neurological deficits. Of the nine patients who had pre-operative seizures, three improved, five did not improve, and one died. Overall, as of the paper’s publication, only eight of the twenty patients had survived beyond infancy, with five now into adulthood (ages 18 – 26) [170]; two of the adult survivors were severely disabled at the time of the report, both having a Karnofsky score [224] of just 40%.
Also worth noting from Table 2 are the six studies in which only patients with dysembryoplastic neuroepithelial tumours (DNETs) were included (Table 3) [61, 62, 94, 132, 182, 184]. These six studies encompass 132 patients, of mean age 9.7 years, amongst whom total tumour resection was achieved in almost 82%, seizure freedom in 87%, and seizure improvement in all but a single patient (99%). However, the adjusted surgical complication rate was slightly higher than that noted across all 26 studies.
Table 4 lists four additional studies of note. Among these four additional studies, three were excluded from the previous table and its summation totals because vascular and other non-neoplastic lesions were intermingled with non-vascular lesions, with no data provided to distinguish between them; and the fourth was excluded because all the patients had tuberous sclerosis, in which brain tubors often cause uncontrolled seizures [225, 226]. The fifteen patients in this fourth study all had subependymal giant cell astrocytomas (SEGA), a tumour that is found in between five and fifteen percent of TS patients [123], typically developing in the region of the foramen of Monro, where it frequently causes obstructive hydrocephalus. Seizures primarily result from a broad array of intra-cerebral tumors, which include the cortical tubers mentioned above, and subependymal nodules, in addition to SEGA [225, 226]. The long-term prognosis therefore is poor, with death primarily resulting from intractable seizures or SEGA-induced obstructive hydrocephalus [225, 226]. As such, it is not unexpected that Cuccia et al. [99] failed to achieve either seizure freedom or any meaningful clinical improvement in seizure frequency in any of their patients. The inherent complexities of SEGA removal, given the relative inaccessibility of these tumours, also could account for the high complication rate (6 of 15, 40%).
The three remaining studies [117, 227, 228] involved a high proportion of non-neoplastic lesions that were not analyzed distinctly from neoplastic cases. Mean seizure free rates across the three studies ranged from a low of 56% to a high of 81%, with seizure improvement noted in 81.3% and 92.4% in the two studies in which this outcome was reported [117, 227]. Although no deaths were reported, almost one in four patients (73 of 320, 22.8%) had a significant post-operative complication, likely due to the highly vascular nature of many of the lesions and the increased risk of intracranial bleeding.
According to the 30 studies (26+4) analysed above, the rate of post-operative complications among patients with epileptogenic brain tumours is low, likely somewhere between 10 and 20 percent, depending upon the nature of the tumour resected, its location, and perhaps other factors as well. The risk of peri-operative mortality also appears to be exceedingly low, with not a single surgery-related death reported among those 873 patients.
Few papers have been published on the post-operative management of paediatric brain tumour patients. What has been reported is that youths tend to experience different intra-operative and post-operative complications than adults, and that these complications affect both short and long-term outcomes, including disability, mortality and hospital and PICU lengths of stay and, hence, direct health care costs [229, 230]. Among the various risk factors for complications are fluid and electrolyte imbalances, which may be especially significant in children. One also must consider that volume of blood loss is all relative to the age and size of the child, given that a human’s total blood volume varies dramatically relative to their age and size: falling from roughly 85 to 90 ml per kg in term neonates, to roughly 85 ml/kg in infants, 80 ml/kg in children under age 10, 70-75 ml in children > 10 and adolescents, and 70ml/kg in adults [231, 232]. Clearly then, 100 ml of blood loss may mean nothing to an adult, but may represent 25% or more of the total blood volume of a newborn.
In general, the most common fluid and electrolyte abnormalities observed after brain surgery in children relate to serum sodium levels, with hyponatraemia secondary to either the syndrome of inappropriate diuretic hormone (SIADH) secretion or cerebral salt wasting syndrome, and hypernatraemia caused by diabetes insipidis (DI) [233-236]. In one series of 79 children, for example, water and sodium disorders were noted in 36 (46%): 23 (29%) with DI, 12 (15%) with SIADH, and a single patient with cerebral salt wasting [236]. Why this is especially important in the paediatric patient in whom an epileptogenic brain tumour has been resected is that sodium disturbances are a significant risk factor for seizures. In one study involving 223 paediatric patients with epileptic brain tumours undergoing 229 surgical procedures, post-operative hyponatraemia — due to either SIADH or cerebral salt wasting — was one of just three independent factors associated with peri-operative seizures, the other two being a supratentorial tumour and patient age less than two years [179].
In another study of 105 paediatric patients post brain tumor resection admitted to the PICU, patients required an average of 0.7 unexpected intensive care unit interventions, mostly secondary to sodium abnormalities, followed by new neurologic deficits, paresis, and seizures [237]. Interestingly, however, 68% of the patients were stable enough to be transferred out of the PICI within 24 hours of surgery.
With respect to anti-epileptic drugs, the same applies post-operatively as pre-operatively, in that there is generally no need to initiate AEDs in patients who have not yet experienced seizures, given the lack of evidence documenting any benefit of prophylaxis [180, 238]. This being said, there are no clear guidelines as to when and how to discontinue AEDs if they have been initiated pre-operatively, and there is always the potential risk of withdrawal-induced seizures [59]. In one study of 332 mostly adult patients, but including some as young as age 16, among those with AEDs that had been initiated to treat seizures pre-operatively, patients with a longer history of seizures (p<0.001) and those with simple partial seizures (p=0.004) were found to be especially likely to continue to have seizures in the immediate post-operative period, as well as poorer control long-term [58]. If AEDs are started post-operatively to reduce the risk of seizures following the trauma of surgery in a patient who otherwise has not had seizures, they generally should be administered short-term [239].
In virtually every series we have reviewed, patients were described who underwent resection of their epileptogenic brain tumour, with apparently successful removal of the tumour, yet no achieved control of seizures. Additional patients were noted to suffer from the post-operative onset of new seizures [170]. And still others had complete control of their seizures, only to relapse later, either while still on an anti-epileptic drug or after all AEDs had been withdrawn. Each of these three scenarios has implications with respect to patient prognosis and management.
The clinical implications of seizures that either start or re-start months or years after the initial resection of tumour are somewhat different than seizures that start immediately post-operatively or that started pre-operatively and failed to resolve with surgery. The major concern with the latter two scenarios is that tumour resection either was incomplete, or that extra-tumoral epileptogenic tissue was not removed. Over the years, attempts have been made to optimize the resection of epileptogenic lesions by both better delineating their margins and identifying extra-tumoral epileptogenic tissue, using intra-operative tools like electrocorticography (ECoG) to identify potential seizure-inducing tissue irregularities like cortical dysplasia [63, 77, 93, 132, 1 [6]3, 184, 214, 216, 240, 241]. This has led to debate regarding the relative benefits and safety of performing epilepsy surgery rather than just lesionectomies in patients with tumour-triggered seizures [242]; though, in fact, many surgeons have been utilizing additional surgical steps like lobectomies, amygdylohypocampectomies and, in extreme cases, hemispherectomies for decades [63, 86, 94, 117, 132, 148, 149, 168, 182, 185, 214, 217, 218, 222, 227, 243]. To date, almost no direct empirical comparisons have been undertaken. In perhaps the most methodologically sound study, Gelinas et al. retrospectively compared 34 patients who underwent ECoG-aided epilepsy surgery and 33 patients who had undergone simple lesionectomies without ECoG, all between the ages of 3 months and 16 years, in Vancouver, Canada [214]. One year post-operatively, the two treatment arms were virtually identical, with roughly 80% of patients in each group seizure free. However, at a mean follow-up of 5.8 years, there was a trend towards improved seizure freedom in patients in the ECoG group, with 79% versus 61% patients still seizure free (p=0.08). The investigators also noted no increase in neurological morbidity among patients who had undergone the more extensive ECoG-guided cortical resection, and that these patients were less likely to require repeat epilepsy surgery [214]. Why this has implications post-operatively relates to the potential need for re-operation, as discussed in the next section.
If the major concern of continued seizures is residual tumour or other epileptogenic tissue, the major concerns with later tumour recurrence are multiple. They include the possibility: (1) that the tumour itself is re-growing, having never been fully resected; (2) that the tumour has undergone malignant transformation; or (3) that some secondary tumour has started to develop, perhaps as a consequence of brain irradiation, chemotherapy, or some other cause. The risk of second brain malignancies is especially high in patients with CNS tumour-associated familial syndromes like neurofibromatosis types 1 [121] and 2 [122], tuberous sclerosis [123], von Hippel Lindau disease [244, 245], and basal cell nevus syndrome [246], with some of these tumours originating within the brain and others the result of metastatic spread from some extra-cranial site. All of the above-mentioned scenarios warrant investigation, which will include diagnostic imaging, due to their potentially dire consequences
Re-growth of tumour is anticipated among children with high-grade lesions, especially glioblastomas [81, 146, 247]. However, although long-term prognoses remain dismal, small improvements in survival times are being reported even among patients with GBMs, relating to advanced surgical techniques, the introduction of real-time, intra-operative imaging and brain mapping, and combining TMZ with radiation therapy [147, 189, 247-250]. Recall that in one study in which eleven of the 20 children had either a grade III or grade IV lesion, including two GBMs, a grade IV PNET, and a grade IV neuroblastoma, all 20 patients lived beyond four years [35]. Nonetheless, when the return of seizures leads to the discovery of grade IV tumour progression, surgery is almost never indicated. Instead, radiation therapy, chemotherapy, or both can be used and may be effective at reducing seizures [81, 208]. The recurrence of seizures does not necessarily indicate tumour progression, however. Sometimes, intrinsic changes within the tumour itself render AEDs less effective, so that switching or combining drugs may be beneficial [72]. As mentioned in Section 3, in such cases, care must be taken to avoid interactions between chemotherapeutic and anti-epileptic drugs [109].
Tumour re-growth also in anticipated in many low-grade gliomas and other neuroglial tumours when total resection is not achieved, and this can be manifested by the recurrence or worsening of seizures. This being said, malignant transformation has been documented with virtually every form of low-grade brain tumour, especially low-grade gliomas [65, 68, 112, 131], but also traditionally-benign lesions like DNETS [64, 67, 209-211], gangliogliomas [209, 212], meningiomas [251, 252], vestibular schwannomas [251], pituitary adenomas [251], and haemangioblastomas [251], among others. Glioblastomas have even been documented to arise at the site of previously totally-resected tumours [253]. Previously-controlled seizures generally are harder to control once malignant-transformation has occurred, even independent of tumour size or rate of progression [78]. Identification of such transformation therefore has implications in terms of patient prognosis, and management of both the tumour and the seizures.
Finally, the late recurrence of seizures can represent the formation of a secondary tumour, perhaps induced by brain irradiation or chemotherapy [251].
Whether seizures start immediately after surgery, later along in follow-up, or never fully remit, in all three scenarios, some patients will have seizures that remain uncontrolled despite the use of AEDs. In our review of the 26 studies listed in Table 2, as well as in various other case series and case studies, we found that, occasionally, patients undergo second or even third resections to remove either residual tumour that is now identified on post-operative imaging, or a residual or newly-identified epileptogenic focus. Though sometimes prolonged attempts are made to control the seizures with medication prior to the second surgery, in some cases, surgery is almost immediate, even within a few days of the initial procedure [254]. In one multi-centre survey that involved 116 children under age 3 undergoing epilepsy surgery for a variety of causes, 27 children were brought into the operating room for a second procedure, and six of these for a third procedure to control seizures [171]. Both the approaches and results of these second operations are mixed. In terms of the former, attempts are usually made to resect any residual or newly-discovered tumour, as well as to identify and resect other epileptogenic foci. Approaches range from simple lesionectomies to lobectomies and, in the most severe cases, hemispherectomies [243].
Table 5 summarizes ten studies we identified, published over the past two decades, in which second operative procedures were performed [46, 77, 157, 1 [6]2, 171, 216, 242, 254-256]. Half of these studies were exclusive to paediatric patients, while the other half included children, adolescents and adults. The study by Steinbok et al. was restricted to infants under the age of 3 years at the time of their initial surgery [171]. In this study, six of the patients required a third surgical procedure prior to achieving their final seizure outcome. Follow-up for most of these studies was approximately two years, but sometimes not reported. Overall, slightly less than half of the patients (46%) achieved seizure freedom, with roughly half the remainder (where reported) achieving at least a significant reduction in seizures. As with the first procedures, operative mortality was low, with only one death in 132 patients and 138 procedures.
A brain tumour is identified in one to three percent of non-febrile seizures that occur in a child. Meanwhile, seizures occur in between one in ten and one in five paediatric patients with a brain tumour, often as a presenting symptom. Most are associated with low-grade gliomas, like pilocytic astrocytoma, or with neuroglial tumours like ganglioglioma or dysembryoplastic neuroectodermal tumour (DNET). There is no empirical justification for initiating an anti-epileptic drug in a brain tumour patient without seizures, and some would restrict their use to those patients who experience at least two ictal episodes.
The cornerstone of management in most patients with a low-grade lesion is surgical resection, both because doing so often prolongs survival and reduces or eliminates seizures. Overall, almost 80% of children who undergo surgery to for resection of an epileptogenic brain tumour will attain prolonged seizure-freedom, and more than 90% will experience at least some meaningful clinical improvement, associated with a negligible risk of death in experienced surgical hands. Risks may be greater and results poorer in very small infants (under one year of age), but most-preschool children can undergo epilepsy-lesion resections safely and with benefit. Significant surgical complications occur in 10-20% of patients and include fluid and electrolyte imbalances, as well as typically short-lived neurological deficits in most patients, so that vigilant post-operative monitoring is essential.
Late post-operative seizure recurrence is an ominous sign that can be a harbinger of tumour recurrence, progression, or malignant transformation, as well as the appearance of new tumours, especially in patients with familial tumour syndromes like neurofibromatosis and tuberous sclerosis, and those who have received brain irradiation. When low-grade tumours recur and cause seizures, second resections may be effective at again controlling seizures.
These claims must be interpreted with caution, however, given that many essential questions remain unanswered — like whether more extensive epilepsy surgery is more effective or as safe as lesionectomy alone; and what factors best predict outcomes. In addition, with the emergence of new anti-epileptics, new anti-neoplastic treatments, and new surgical technologies, the management of epilepsy in children and adolescents with brain tumours appears to be rapidly changing.
\n\t\t\t\tAED\n\t\t\t | \n\t\t\t\n\t\t\t\tInteractions with\n\t\t\t | \n\t\t
Phenytoin | \n\t\t\tcarboplain, cisplatin, cyclophosphamide, dacarbazine, erlotinib, etoposide, fluorouracil, | \n\t\t
\n\t\t\t | ifosfamide, imatanib, irinotecan, carmustine, lomustine, paclitaxel, | \n\t\t
\n\t\t\t | procarbazine, tegafur, teniposide, thiotepa, topotecan, vincristine | \n\t\t
Carbamazepine | \n\t\t\tcisplatin, cyclophosphamide, erlotinib, etoposide, ifosfamide, imatinib, irinotecan, | \n\t\t
\n\t\t\t | carmustine, lomustine, palitaxel, procarbazine*, teniposide, thiotepa, topotecan, vincristine | \n\t\t
Phenobarbitol | \n\t\t\tcyclophosphamide, erlotinib, etoposide, ifosfamide, imatinib, irinotecan, carmustine, | \n\t\t
\n\t\t\t | lomustine, paclitaxel, procarbazine, teniposide, thiotepa, topotecan, vincristine | \n\t\t
Primidone | \n\t\t\tcyclophosphamide, erlotinib, etoposide, ifosfamide, imatinib, irinotecan, carmustine, | \n\t\t
\n\t\t\t | lomustine, paclitaxel, procarbazine, teniposide, thiotepa, topotecan, vincristine | \n\t\t
Valproic Acid | \n\t\t\tcisplatin, cyclophosphamide, vorinostat | \n\t\t
Anti-epileptic drugs (AED) and their interactions with CNS anti-neoplastic drugs
*Carbamazepine is contraindicated in patients on procarbazine
\n\t\t\t\t | \n\t\t
Seizure response to surgical resection of epileptogenic tumor
* Some patients died before final seizure assessment; ** Three patients underwent a second reaction; *** These 16 patients part of a larger series with other seizure aetiologies included
GG=ganglioglioma; DNET=dysembryoplastic neuroepithelial tumor; PGNT=papillary glioneuronal tumor; LGG=low-grade glioma; ODG=oliogodendroglioma; AC=astrocytoma; CPP=choroid plexus papilloma; CP=craniopharyngioma; L=lesionectomy; L+E=lesionectomy+additional resection of adjacent epileptogenic tissue; L+A=lesionectomy+amygdylohypocampectomy; L+L=lesionectomy+lobectomy; TL=temporal lobectomy; L+L+A=lesionectomy+lobectomy+amygdylohypocampectomy; AHC=amygdylohypocampectomy; (T)=all temporal lesions
\n\t\t\t\t | \n\t\t
Seizure response to surgical resection of dysembroplastic neuroectodermal tumors
\n\t\t\t\t | \n\t\t
Seizure response to surgical resection of epileptogenic tumor – studies including vascular lesions
Vasc=vascular lesions; SEGA=subependymal cell astrocytoma; TS=tuberous sclerosis; FU=follow-up
\n\t\t\t\tFirst\n\t\t\t | \n\t\t\t\n\t\t\t\tYear\n\t\t\t | \n\t\t\t\n\t\t\t\t#\n\t\t\t | \n\t\t\t\n\t\t\t\tMean\n\t\t\t | \n\t\t\t\n\t\t\t\t#\n\t\t\t | \n\t\t
\n\t\t\t\tAuthor\n\t\t\t | \n\t\t\t\n\t\t\t\tPublished\n\t\t\t | \n\t\t\t\n\t\t\t\tSubjects\n\t\t\t | \n\t\t\t\n\t\t\t\tAge (y)*\n\t\t\t | \n\t\t\t\n\t\t\t\tSeizure Free\n\t\t\t | \n\t\t
Benifla | \n\t\t\t2006 | \n\t\t\t12 | \n\t\t\t13.5 | \n\t\t\t7 | \n\t\t
Chae | \n\t\t\t2001 | \n\t\t\t1 | \n\t\t\t0.3 | \n\t\t\t1 | \n\t\t
Gonzalez-Martinez | \n\t\t\t2007 | \n\t\t\t57 | \n\t\t\t24.7 | \n\t\t\t22 | \n\t\t
Im | \n\t\t\t2002 | \n\t\t\t3 | \n\t\t\t16.5 | \n\t\t\t3 | \n\t\t
Jooma | \n\t\t\t1995 | \n\t\t\t8 | \n\t\t\t24.0 | \n\t\t\t5 | \n\t\t
Lombardi | \n\t\t\t1997 | \n\t\t\t1 | \n\t\t\t? | \n\t\t\t1 | \n\t\t
Ojemann | \n\t\t\t2012 | \n\t\t\t4 | \n\t\t\t8.5 | \n\t\t\t2 | \n\t\t
Steinbok | \n\t\t\t2009 | \n\t\t\t24 | \n\t\t\t1.5 | \n\t\t\t12 | \n\t\t
Tian | \n\t\t\t2011 | \n\t\t\t9 | \n\t\t\t13.7 | \n\t\t\t3 | \n\t\t
Whittle | \n\t\t\t1995 | \n\t\t\t4 | \n\t\t\t36.0 | \n\t\t\t0 | \n\t\t
Totals | \n\t\t\t\n\t\t\t | 123 | \n\t\t\t\n\t\t\t | 56 | \n\t\t
Mean | \n\t\t\t\n\t\t\t | \n\t\t\t | 15.4 | \n\t\t\t\n\t\t |
Percentages | \n\t\t\t\n\t\t\t | \n\t\t\t | \n\t\t\t | 45.5% | \n\t\t
Seizure response to a second surgical resection
Malaysia is the world’s second largest exporter of palm oil (Figure 1) with approximately 5.08 million ha of land under cultivation [1]. Major percentage of these plantations is owned by small-scale private farmers that have huge demands to affordable low-cost autonomous platforms for applications, such as scouting, palm census, yield monitoring, spraying, and most importantly health assessment and disease detection. The ability to collect high spatial resolution aerial images using drones is changing the way the oil palm growers are approaching the business [2]. Conventional methods of practicing precision agriculture (PA) in oil palm plantations such as remote sensing and spraying are being replaced by integrated fixed-wing or multirotor unmanned aerial vehicles (UAV) [3], allowing collection of information to be instantly accessible for immediate decisions. Precision farming for increasing oil palm yield requires optimization of returns on inputs while preserving resources based on sensing, measuring, and health assessment of the plantations [4]. Relying on satellites images of palms, there is a substantial lag in terms of accessing the data quickly enough. Professionals have been using satellite and piloted airplane remote sensing platforms [5] for plantation scouting applications, such as vegetation cover assessment [6], vegetation mapping [7], crop monitoring [8], and forest fire applications [9]; however, the difference that drone technology [10] and agricultural robotics [11, 12, 13] have made is around the speed and accuracy of delivering that information. Digital agriculture [4] offers great opportunities for mechanization and automation of farming tasks in oil palm plantations through automation of data collection by means of ground or aerial surveillance and data processing software to predict or estimate palms yields.
Comparison between world exports of palm oil, with Malaysia as the second largest exporter. (data: [1]).
Conventional scouting of oil palms on a regular basis (Figure 2), as well as palm census and quantification of the amount of fresh fruit bunches (FFB) for yield monitoring, is a labor-intensive task that is either ignored or carried out manually by the use of hand counters. Traditional scouting of palms is an ineffective practice that requires expert knowledge and postprocessing lab equipment. It involves spending hours and hours of human observation inside the unpleasant hot and humid plantation and does not provide accurate and comprehensive information because several parameters are ignored due to measurements difficulties (i.e., tasks that involve climbing trees, measuring canopy diameter, etc.). Other than the inaccuracy and biases statistics, manual scouting involves additional costs for each extra observation, hazards, and safety issues (i.e., falling from trees, bugs, snake bites, etc.). Satellite imaging services are extremely costly, and they can take images only once a day and have to be ordered in advance. The resolution of these images is low and can be influenced greatly with certain sky cloud conditions. Ground sensing platforms are also time consuming and are limited to small fields of view. Yield reduction due to high-density palm areas that cause etiolation is an issue in plantation management. Palm densities are an important and limiting factor for growth, nutritional status, fruiting, and hence for the plantation yield. Optimal palm densities depend on different factors, such as cultivars, climate, soil characteristics, and land preparation. Refilling of palm gaps and correction of nonoptimal densities are of high priority for a good plantation management. Conventional methods that are solely based on visual observation are inaccurate, particularly when coverage is large and dominant topography is hillocky.
Tedious field work with conventional scouting of oil palm plantation.
Precision agriculture of oil palm is one of the largest markets in Malaysia that will be hit by UAV and robotics. These devices are the future of PA and are sometimes referred to as the next step in data-driven agriculture. UAV/drones carrying multi-spectral and multimodal data acquisition devices face adaptation challenges to satisfy information, accuracy, and timeliness as the bases of a successful precision agriculture (PA) operation. These platforms have contributed to significant reductions of in-field walking costs and observational experiments. UAVs are defined as “an aircraft that is equipped with necessary data processing units, sensors, automatic control, and communications systems and is capable of performing autonomous flight missions without the interference of a human pilot” [14]. The global market for agricultural UAV drones is estimated to reach 3.7 billion US dollars by the year 2022 (Source: Radiant Insight Research firm). Aerial photography from UAS has bridged the gap (see the schematic diagram shown in Figure 3) between ground-based observations and remotely sensed imagery of conventional aircraft and satellite platforms and has made possible great improvements in crop scouting, yield mapping, field boundary mapping, soil sampling and soil property mapping, weeds and pest control and mapping, vehicle’s guidance, navigation control, and spraying. These devices are easy to use and are typically flexible, low cost, light-weight, and low airspeed aircraft. They have revolutionized smart farming and precision agriculture, from planting to harvesting, from seeding to sensing, and from scouting to spaying. UAS drones are widely available on demand, and their functionalities can be customized for different farming applications and can provide a cost-effective monitoring platform without requiring an expert operator. With this technology, several problems associated with the data resolution from piloted aircraft and satellite imaging have been solved. They are capable of providing live data from a wide range of sensors, such as those shown in Figure 3 (multispectral, NIR, LiDAR, etc.) at precision resolutions measured as centimeters per pixel. Such information contributes to the in-depth analysis for the crop health assessment or the inventory management databases. With the UAV technology, the following can be achieved: information about accurate planted area for replanting or thinning, palm census for creating inventory database, calculating the total land area in use, finding distances between each palm to specific spots, calculating canopy diameter, palm height, and palm density, creating 2D, 3D, GIS, NDVI maps for plantation, identifying palm status based on Orthomosaics and digital elevation models, detecting healthy and unhealthy palms (stress assessment), monitoring exposed soil for variable rate technology application, quantification of fresh fruit bunches and mature fruits for yield calculation, monitoring chlorophyll content and nutrient estimation, and measuring leaf area index, drought assessment, biomass indication, weed detection, and inventory management. Data and information such as these are useful for developing decision support systems and yield prediction models.
Typical components of a UAV-based remote sensing platform for precision agriculture of oil palm.
UAV drones can be well adapted for oil palm plantations, where field work is tedious. They allow observation of individual palm trees and can operate unnoticed and below cloud cover that prevents larger high-altitude aircraft and satellites from performing the same mission. Moreover, they can be deployed quickly and repeatedly, and they are less costly and safer than piloted aircraft, are flexible in terms of flying height and timing of missions, and can obtain very high-resolution imagery. As an aerial remote sensing platform, a UAV drone must be adapted to satisfy the basic requirements of image data collection from oil palm plantation. Other than the selection of proper sensors, the stability and accuracy are vital to provide geo-referenced images for extraction of useful information. Adaptation of UAV technology for oil palm plantations involves integration of vision sensors, machine vision algorithms, and control system for (i) yield monitoring and yield mapping, (ii) automated airborne pest monitoring using thermal cameras, (iii) identification and counting of specific insects from very high-resolution optical images, (iv) development of decision support system (DSS) using geo-referenced images as a basis for a GIS-based system giving oil palm growers the possibility to incorporate data directly to their precision farming platforms, (v) identification and mapping of Ganoderma disease using hyperspectral camera, (vi) automated retrieving of oil palm canopy chlorophyll and nutrient content from multispectral and hyperspectral UAV acquired images, and (vii) dynamic Web mapping and inventory management of oil palm productivity using in situ sensors. This paper is the first of series reporting on design and development of an affordable fixed-wing UAV to be used as a flexible scouting test bed for oil palm plantations. Schematic diagram illustrating the early stages of technological development for introducing a UAV platform to local farmers and the general steps and procedure involved with setting up a UAV remote sensing platform for agricultural applications are shown in Figures 4 and 5, respectively.
Schematic diagram illustrating the early stages of technological development for introducing a UAV platform to local farmers (source: Adaptive AgroTech Consultancy International).
General steps and procedure involved with setting up a UAV remote sensing platform for agricultural applications.
A comprehensive document including recommendation for choosing the best UAV drone for precision agricultural and smart farming applications is available in [15]. Specifications of sample multirotor and fixed-wing UAV recommended for precision agriculture of oil palm are also provided in the Appendix. Compared with piloted airplanes and satellite imaging, the ability of UAVs in collecting higher resolution aerial images at a significantly lower cost can provide oil palm growers with more accurate information on palm height, crown size, and normalized difference vegetation index (NDVI), enabling practicing of data-driven techniques for early and accurate yield estimation and health assessment. While a typical UAV may cost as little as USD1000, it can be integrated with custom instrumentations, controllers, sensors, and software to operate as a flexible remote sensing or variable rate technology platform to contribute to plantation management, growth, and soil condition assessment mapping application (i.e., 2D, 3D, GIS, NDVI), risk/hazard/safety management, spraying application, and academic and research application. In specific, UAV remote sensing in oil palm precision agriculture can contribute to automatic palm detection and counting, automatic measurements of palm height and crown diameter measurements, calculation of planted and unplanted areas for replanting or thinning, analyzing palm status based on Orthomosaics and digital elevation models, inventory management and health assessment based on physical appearances and vegetation indices, model-based yield prediction, yield monitoring and mapping, rapid estimation of nutrient contents, and disease detection. It should be noted that agricultural UAV activity is considered commercial operation with a high-tech platform for data acquisition or spraying applications that should be carried out by licensed professionals or certified pilots. Price range for a complete package is between USD1500 to over USD25000 depending on the application. Multicopter drones can fly for 3–45 minutes on a one battery charge and are more suitable for regular use in small-scale plantation without the requirement to special takeoff and landing areas. Fixed-wing UAVs need to be planned for mission flights and reliable landing for use in larger plantations. It is better to purchase drones that can be controlled via mobile or tablets or are fully autonomous from takeoff to landing (i.e., the entire mission can be performed by a single start button). For a multicopter, it is also important to check for the live standstill view feed. This feature allows plantation managers to find specific spots and issues for closer inspection. One of the key considerations in purchasing scouting UAV is the NDVI and NIR camera options. For the sake of cost saving, an affordable regular 3D camera with two lenses can be purchased for less than USD300 and modified slightly with a blue plastic filter to produce NIR images. However, a more expensive UAV that can collect data faster will compensate the extra costs in a long run.
Health assessment in oil palm plantations is crucial for spotting fungal infection and bacterial disease on the palms. By aerial scanning the plantation using visible RGB camera, NIR, hyperspectral, and multispectral sensors, it is possible to identify temporal and spatial reflectance variations before they can be detected by naked eyes and associate these changes with palms heaths for an early response. For instance, NDVI cameras can calculate the vegetation index describing the relative density and health of the palms, and thermal camera can show the heat signature of different spots in the plantations. A conceptual demonstration of a UAV remote sensing platform equipped with NDVI sensor for oil palm health assessment is shown in Figure 6.
Conceptual demonstration of a UAV-remote sensing platform for oil palm health assessment with NDVI camera.
The platform shown in Figure 7 can be customized and integrated with hyperspectral camera as shown in Figure 8, for the detection of Ganoderma boninense, which is a serious threat to oil palm plantations in Malaysia and has caused great losses to healthy palms. This disease causes both basal stem rot and upper stem rot and remains South East Asia’s most devastating oil palm diseases, with direct loss of the stand, reduced yield of diseased palms, and the resultant requirement for earlier replanting. Using naked eye, the Ganoderma disease can only be recognized at a very late stage with serious symptoms of foliar chlorosis and breakage at older fronds, the presence of decayed tissues at palm base, and production of fruiting bodies. When symptoms of the disease appear on young palms, it is too late and younger palms die within 6 to 24 months, whereas mature palms may survive for 3 years. Reports also indicate that the basal stem rot can kill up to 80% of the total standing palms. Despite the several efforts in controlling this disease, the available methods are slow, and current strategies are still immature. To our knowledge, no effective method or a robust sensing instrumentation has been commercialized for early detection of this disease at an early stage. Research reports have highlighted that oil palm yields are highly correlated with most of the nutrients. There are extensive publications on the hyperspectral analysis of images with application in agriculture that shows promising methods to be adapted for early detection of Ganoderma disease in oil palm. In order to adapt a UAV remote sensing platform for this purpose, several questions should be addressed as follow: (i) at what stages of infection can the hyperspectral imaging detect the Ganoderma disease symptoms? (ii) what are the unique spectral characteristics of Ganoderma spectral reflectance data? (iii) what statistical or mathematical methods are the best for analyzing the Ganoderma spectral data? and (iv) how well can a low-cost multiband radiometer assist a scouting crew to detect the suspicious HLB-infected trees? We can begin with a hypothesis that wavelet analysis of reflectance data can improve detection of nutrient concentration in oil palm. This hypothesis can be studied by the use of the Matlab Wavelet CIR images Toolbox. Preliminary studies have demonstrated the potential of wavelet analysis for retrieving foliar nitrogen content and photosynthetic pigment concentrations from leaf and canopy reflectance spectra, but further research is needed to develop the approach. Our research will contribute to saving of more palm trees and consequently a higher yield which has a significant impact on large scale plantations and the economy of Malaysia. A project can be proposed with the long-term goal of developing a fast UAV-based screening technique that can assist oil palm growers in detecting suspicious Ganoderma-infected palms. Such a project may involve the following systematic steps and methodology: (i) study the spectral characteristics of GB in lab conditions, (ii) developing a classification method to identify the disease and separate it from other palm stresses and other diseases with similar symptoms, (iii) evaluating the possibility of using a low-cost spectral radiometer for fast screening of Ganoderma-infected palms, (iv) developing an instrumented platform for collecting and geo-referencing hyperspectral images in the plantations, and (v) conducting a field trial to evaluate the effectiveness of hyperspectral imagery for detecting the disease in the plantations. Reflectance spectra of vegetation, measured in the visible and infrared region, contain information on plant pigment concentration, leaf cellular structure, and leaf moisture content. In this research, we propose to study the capability of hyperspectral imaging and spectroscopy in the range of 300-2500 nm for early detection of anomalies in oil palm trees as a result of Ganoderma infection. Preliminarily hyperspectral imaging data indicated that Ganoderma-infected leaves have different spectral characteristics compared to healthy leaves. A quick and efficient method of detecting and mapping Ganoderma at the field level will assist growers to better manage and control this disease and can financially benefit growers. In the first year of the study, we will study the spectral characteristics of Ganoderma-infected oil palm leaves in laboratory conditions and compare them with other nutrient deficiency symptoms. Accordingly, we will develop a classification method to identify the symptoms of Ganoderma and separate it from plant stresses and other diseases with similar symptoms. Also, in the first year, we will study how well a low-cost spectral radiometer can detect Ganoderma symptoms. Based on the results from the first year of the study, we will develop an instrumented platform for collecting and geo-referencing hyperspectral images and evaluate the effectiveness of hyperspectral imagery for detecting suspicious Ganoderma-infected palm trees in the grove.
Feasibility of using autonomous UAV-based hyperspectral imaging for detection of Ganoderma boninense disease in oil palms.
Thermal camera and night vision (top row figures) and high-resolution RGB images approach (bottom row figures) for UAV based pest monitoring in oil palm plantations.
Oil Palm growers lose some portion of their yields to insects and pests infestation. Traditional methods of locating pests in thousands of hectare plantations are not effective. For example, early detection of an invasive pest like rats in palm plantations with labor requires a great amount of time and luck. Obviously, conventional methods are not accurate, and plantation managers have to make an educated guess before sending the crew to a large field to check for infested spots. For the purpose of pest monitoring, a solution is to have a UAV imagery platform equipped with a thermal camera and high-resolution RGB vision sensors for accurate identification of the spots in the oil palm plantations fields that are diagnosed with specific insects and pests. This approach may also involve development of a decision support system (DSS) using georeferenced insect count as a basis for a GIS-based system, giving plantation managers the possibility to incorporate data directly to their precision farming platforms. Specific steps involve (i) platform setup, that is integration of the UAV, vision sensor, and control system, (ii) perception which refers to the development of a real-time machine vision algorithm for pest monitoring (to refine the aerial images captured by the UAV in order to provide plantation managers with the most usable data), and (iii) action stage, which is the development of the DSS for creation of the prescription map. When pests are spotted, spraying UAV can be used for dropping a targeted load of pesticide. The spraying UAV can be equipped with distance-measuring and light detection sensors such as lasers, ultrasonic echoing, or LiDAR methods to scan the ground and adjust the flight altitude with the varying topography of the plantation and therefore apply the correct amount of spraying liquids for even coverage and avoid collisions. This practice will result in an increased efficiency while reducing the amount of penetrating spray chemical in the soil and groundwater. It is estimated that UAV spraying is five times faster than conventional tractor and machinery equipment.
The FLIR Vue Pro thermal camera shown in Figure 8 is designed for small UAVs and can be used for agricultural applications. It has different lens options for different type of view and specific applications. The thermal sensor resolution of this camera is 640 by 512 pixels and records 30 frames per second for smooth video. The light weight and small size of this camera will not affect the UAV center of gravity during the flight or sacrifice the flight time. It comes with the mounting accessories that can be used with most UAV platforms. It can also be used with transmitters for live feeds. The FLIR Vue Pro thermal camera does not have a separate battery and can be charged through a 6 V power from the UAV. Image data are stored on a standard micro SD card. An application connects the camera with the computer via Bluetooth. The thermal imager Optris PI 640 shown in the figure is the smallest measuring VGA infrared camera available. With an optical resolution of 640 × 480 pixels, the PI 640 delivers pin-sharp radiometric pictures and videos in real time. With a body sized 45 × 56 × 90 mm and weighing only 320 grams (lens included), the optris PI 640 counts among the most compact thermal imaging cameras on the market. Temperature range is between −20 and 900°C (optional up to 1500°C), spectral range is between 7.5 and 13 μm, and frame rate up is to 125 Hz. For the purpose of validation, images taken at varying heights and resolutions will be compared with the ground truth pictures taken on the ground with a mobile device. The research findings may lead to new pest management strategies that use UAV and other imaging technologies for detecting invasive pests in other farm fields, e.g., oil palm plantations. The thermal camera can also be used for spotting the areas that are drier and require attention.
Quantification of FFB from UAV stream images for yield map creation is the first step toward practicing PA in oil palm plantations. With the available high-tech imaging sensors and using real-time image processing and remote sensing techniques (i.e., pixel-based or object-based [16], template matching [17, 18, 19] image analysis, learning algorithms methods for classification [20, 21] and for extracting useful information from an image), it is possible to measure oil palm yield on much smaller scales. One of the benefits of using autonomous UAV is their affordable price and lower cost per each mission flight that make them suitable for academic research in yield monitoring applications. The idea is to evaluate the feasibility of having UAV agent robots that can fly over and inside oil palm plantations and collect high-resolution detailed photos from different angles for automated creation of yield maps. These maps can tell growers where and when to apply the optimal amount of inputs (i.e., fertilizer, pesticide, water) for creating further sustainability. Of course, mobile robots with camera and sensors mounted on top of them can also be used for such application; however as mentioned earlier, we are proposing a research idea that involves a swarm or fleet of small-scale UAVs similar to what is shown in the figure that simultaneously fly inside the plantation for image data collection. By using different sensor-based measurement and imaging techniques on each UAV, a real-time machine-vision system can be developed for accurate identification of the amount of FFB on the palms. Such technology is highly demanded by oil palm growers as a fast, accurate, and reliable tool for estimating palm numbers and FFB in large-scale plantations. In determining instantaneous oil palm yield, two parameters must be known, weight and coordination of FFB on each palm. The weight of the FFB can be estimated using a machine vision algorithm that quantifies the number of fruits on each palm (Figure 5). These estimated weights are then georeferenced with coordinates of the corresponding palm using computer programs for the creation of database and yield map. Collected data will be processed by custom-built GIS software for creation of yield map and inventory database. A conceptual illustration of integrated fixed-wing UAV-based inventory management and health assessment system with mobile application and cloud computing is shown in Figure 9.
Feasibility of UAV imaging system for yield monitoring of oil palm (top) and a proposed methodology for UAV-based yield monitoring of apple and orange fruits using deep learning algorithms [22].
One of the limitations of doing research on oil palm plantation is the lack of accurate data and input variables for modeling and simulation purposes. UAV technology can be integrated with image acquisition techniques for three-dimensional reconstruction of the environment and creation of virtual plantations. Examples of 3D reconstructed plantation are shown in Figure 10. The information extracted from these 3D models can lead to the development of dynamic Web inventory management and mapping system. A 3D reconstruction model of oil palm plantation can be created by using range data methods or depth map using laser range finder sensors and 3D scanner instrumentations. This approach is however costly and not affordable by local oil palm farmers. Alternatively, passive methods, also called image-based reconstruction methods (i.e., photogrammetry technique), have been introduced using a normal camera and image sensors, which do not interfere with the reconstructed object. In this method, a UAV equipped with a normal RGB camera will collect images of the oil palm plantations from different views and angles. Computer software will then process these images to create a 3D model, and filter specific wavelength to generate images that corresponds to vegetation index and palm health. For example, a red edge image can describe nitrogen content and water stress. The potential of UAV image data to simulate the physical process of palm photosynthesis as a result of different crown sizes and densities intercepting different amounts of light radiation can be evaluated using virtual plantations. A virtual plantation can be used to estimate palm height, crown size, and inventory database (Figure 11) for generating dynamic Web maps and yield prediction models. These maps can identify how different palm height, crown sizes, plantation densities, and row orientations in different locations can affect the water and fertilizer demand. Moreover, mathematical models can be established based on the validated information from virtual plantations for estimating nitrogen demand and fertilizer application. These maps also provide precision rich data for academic and educational purposes. Researchers can access to detailed measurements of palm trunk and crown size and the spacing between different palms, leaf area index, and crown density as a preliminary study for the possibility of autonomous variable rate applications and robotic harvesting.
Example of virtual plantation generated by UAV imaging [23].
Conceptual illustration of a fixed-wing UAV Web mapping system integrated with mobile application and cloud computing for yield prediction and inventory management in oil palm plantation.
For the purpose of a sensor Web-based approach for dynamic Web mapping, observations from a UAV can be combined with in situ sensor data to derive typical information offered by a dynamic Web mapping service (WMS). This will provide daily maps of vegetation productivity for oil palm plantation with a spatial resolution of 250 m. Results will present the vegetation productivity model, the sensor data sources, and the implementation of the automated processing facility. An evaluation will be made of the opportunities and limitations of sensor Web-based approaches for the development of Web services, which combine both UAV and in situ sensor sources. A conceptual illustration is provided in Figure 11. A yield estimation model can be developed by establishing performing regression analysis between palm height (x1), crown size (x2), palm age (x3), vegetation index (x4), nutrient content (x5), and soil parameters (x6): Yield = func(x1, x2,…, x6). This model will be based on comprehensive information of each palm location, size, and health, will provide managers with an estimation of yield, and make decisions for sustainable practices methods for production increase without necessary needs for expanding the plantation into natural forests.
The fixed-wing Osprey drone shown in Figure 11 is a commercially available, low-cost experimental flight test bed manufactured by Unmanned Aerial Research (Florida, USA) that is suitable for investigating novel control approaches [24] and is a flexible platform for remote sensing research applications in precision agriculture of oil palm. An example application can be found in the work of [25], where the fixed-wing J-HAWK UAV was used for palm tree counting at Melaka Pindah oil palm plantation in Malaysia. This drone can carry large payloads while maintaining excellent performance with virtually no degradation in handling qualities. It is a well-constructed, durable aircraft with mission versatility and a cavernous payload volume that is easily accessible, featuring two long aluminum tracks on the floor for mounting payloads in limitless configurations. Some of the specifications according to the manufacturing website are as follows: payload capacity: 31.75 kg, empty weight: 15.87 kg, payload volume 0.0566 m3 (0.203H × 0.304 W × 0.889 L), max cruise: 90 kts, landing speed (no flaps): 25 kts, power (DA-100): 10 hp by a reliable custom desert aircraft 100 cc motor with 3-blade carbon fiber propeller, wingspan 3.352 mm, and length 2.362 m. We begin with dynamic analysis and controller design for this drone in the presence of actuator limits and sensor noise for autonomous flight missions with greater accuracy and stability. The communication architecture, modules, and designed control system is shown in Figure 12.
Architecture, modules, and control system for a the proposed UAV in precision agriculture of oil palm.
For the purpose of this paper, we have concentrated our analysis on controller design for two outputs, velocity and pitch rate, by adjusting two control inputs, the elevator and the thrust. In specific, our control objective was to design a single controller, i.e., proportional-integral-derivative (PID), Linear-quadratic regulator (LQR) full state feedback, (
where
We first perform open-loop analysis to determine possible control strategies. The open-loop responses (Figure 13) from each of the four TFs were then analyzed individually. According to the TF in (1) and (2), the terms with the highest coupling can be obtained by considering the simple steady state case. Substituting jω = 0, in all the terms, it can be observed that the static gain relationship is high for
Open-loop step response analysis of the Osprey drone velocity and pitch rate for the elevator and thrust inputs.
For the PID controller design shown in Figure 14, the system was set at initial conditions [
Simulink blocks for the PID controller in the absence and presence of noise and actuator limits.
The LQR controller is the solution of the optimization problem that optimizes the cost of errors and the cost of actuation effort, with appropriately weighted states. The optimization function is defined as
Simulink blocks for the designed LQR controller with full state feedback.
It is noted that the control effort for pitch is the most optimized parameter in Q. This value was selected on the basis that pitch is the most influential state variable and controlling pitch translates control of all the other parameters. In addition, the weight for pitch rate is low because the effort to control pitch rate is harder and introduced more oscillations in the system.
For the LQR controller with observer (Figure 16), the observer design allows controller to use full-state feedback techniques in situations where only a subset of states is available to the controller. The observer matrix L adds gain to the feedback loop, in order to ensure stability and quicker response of the state observer system. While this helps stability, the L gain adversely amplifies the sensor noise. Therefore, a trade-off has to be made on the noise resilience versus the system’s robustness. The matrix L was determined through these steps: (i) the system output states were checked for controllability and observability using Matlab code
LQR controller with observer block.
It can be seen that the value of pitch gains in the Q is four times smaller than the previous case. The gains were reduced to take control over noise in the system. In the other words, these reductions help eliminate the noise in the system. From step three of the observer design, we know that the observer matrix L adds gain to feedback loop. This gain helps amplifying the noise and then feeding them into the control loop back again. Noise introduces similar problems faced with the PID controller. With high gains, the noise amplifies and combined with actuator nonlinearities drives the system into instability. With lesser gains and actuator effort, noise is damped and absorbed by the system.
Results of the simulation for the designed controllers are shown in Figure 17 through Figure 20. It can be seen from Figure 17 that the step change applied at time 60 s has an effect on the pitch, and the PID controller is managed to minimize this effect. When noise is introduced to the system (Figure 18), because the coupling gain between pitch and velocity are very high, the pitch rate sensor noise distorts the response considerably. Moreover, since the tuned gains exploited the infinite actuator capabilities, the response of the system was quick and the steady state error was almost zero; however, due to the nonlinearities, the system had to be tuned again. Since elevation was directly related to the pitch rather than the pitch rate and to avoid the dynamics of the “rate” signal, pitch was compared against the elevator angle to generate the error signal. To accomplish this, the pitch rate was simply integrated using an ideal integrator (1/s).
PID performance without noise and actuator limits.
PID performance with noise and actuator nonlinearities.
It can be seen from the results that the state variables pitch and velocity are closely coupled variables. The coupling terms connecting these two quantities exhibit every high gains, hence the control design was challenging in regulating these variables independent of the other. This coupling needed special attention during control design. It should be noted that on the basis of tuning complexity, only two PID controllers were used in the control problem, as if the system was a weakly coupled system. Since PID control is ideally suited for single-input single-output systems (SISO) and only for weakly coupled MIMO systems, a perfect performance was not expected to achieve with the two PID controllers. Nevertheless, a reasonable performance was still achieved when the system was considered ideal, i.e., free from nonlinearities and noise. When noise was introduced to the system, the velocity suffered because of high noise content in the pitch signal. The noise also introduced dangerous oscillations in the system, limiting controller gains significantly and hence slowing down the overall system. Several instabilities caused due to the rate limit and saturation were evident. The integral gain of the PID acted on error build-up caused by saturation and hence pushing the system into instability. After reducing the gains in the loop, the controller was then tuned by trial and error procedures. The relative performance of PID with respect to other controllers is summarized in Table 1.
Model | Price ($) | Weight (Kg) | Size (mm) | Camera resolution | Coverage | Flight time (min) | Max altitude (m) | Flight speed (km/h) |
---|---|---|---|---|---|---|---|---|
Parrot Disco Pro AG Drone | 6875 | UAV: 0.78 Take-Off: 0.94 | Wing span: 1150 × 580 × 120 | — | — | — | — | — |
RF70 UAV | 3000 | Payload: 3 | — | 1080 P | 600 acres/hour | 45–60 | — | 18 |
AgDrone UAS | 10,000 | — | — | 1080 P | — | 60 | — | |
DT-26 Crop mapper | 120,000 | — | — | 1080 P | — | 60 | — | 110 |
Quad Indigo | 25,000 | — | — | 1080 P | — | 45 | — | |
E384 Mapping Drone | 2400 | UAV: 2.5 Payload: 1 | Wingspan: 1900 Length: 1300 | — | 1000 acres in 100 minutes at 5 cm resolution | 90 | — | 47 |
PrecisionHawk Lancaster 5 | — | Payload: 1 | — | 1 cm/pixel | 300 acres/flight | 45 | — | — |
Xena observer | — | Take-Off: 5 | — | — | — | 27 | 5000 | — |
Xena thermo | — | Take-Off: 4.6 | — | — | — | 32 | 5000 | — |
AEE AP10 Drone | 299 | — | — | 1080 P Full HD Video at 60 FPS | — | 25 | 500 | 71 |
UAV drone crop sprayer | UAV: 9 Payload: 10 Take-Off: 13 | 800 × 800 × 70 (L.W.H) | — | — | 16 | 1000 | — | |
DJI drone sprayer | 15,000 | — | — | — | 7–10 acres/hour | — | — | 29 |
Yamaha’s helicopters spray & survey | 130,000 | UAV: 71 Payload: 30 | — | — | 10 acres | — | — | — |
JMR-V1000 6-rotor 5 L | 665–3799 | UAV: 6.5 Take-Off: 18 | 875 × 1100 × 480 (L.W.H) | — | — | 14–18 | — | 11–22 |
AG-UAV Sprayers1 | — | UAV: 8 Payload: 6 | Height: 650 | — | — | 8–15 | — | — |
AG-UAV Sprayers2 | — | UAV: 14.2 Payload: 20 | Height: 650 | — | — | 15–30 | — | — |
AG-UAV Sprayers3 | — | UAV: 9.5 Payload: 10 | Height: 650 | — | — | 10–20 | — | — |
DJI AGRAS MG-1 Sprayer | 7999 | Payload: 10 | — | — | 7–10 Acres Per Hour | — | — | — |
Hercules Heavy Lift UAV (HL6) | — | UAV: 8 Payload: 6 | Height: 660 | — | — | 30 | — | 37 |
Hercules Heavy Lift UAV (HL10) | — | UAV: 9.5 Payload: 10 | Height: 660 | — | — | 30 | — | 37 |
Hercules Heavy Lift UAV (HL20) | — | UAV: 14 Payload: 20 | Height: 660 | — | — | 60 | — | 37 |
Multirotor UAVs | — | — | — | — | — | 10–40 | — | — |
AgStar GoPro FPV Camera Payload | 1950 | — | — | — | — | — | — | |
DJI Phantom 3 | 469 | — | — | 2.7 K HD videos, 12 MP photo | — | 25 | — | — |
Fixed Wing UG-II | — | UAV: 11 Take-Off: 15 | 2240 × 1600 × 650 (L.W.H) | — | — | 180 | — | 65–110 |
Professional Electric Six Rotor Drone UA-8 Series | — | Payload: 3 | 860 × 860 × 540 | — | — | 28 | 5000 | 36 |
Yuneec H520 Hexacopter | 2500–4500 | — | — | 4 K/2 K/HD video or 20 MP images | — | — | — | — |
Ag-drone AK-61 | 6999 | Take-Off: 22 Payload: 10 | — | — | — | 10–15 | 0.5–5 m | 18–36 |
YM-6160 | 5000 | Take-Off: 21.9 Payload: 10 | — | — | — | 10–15 | 0.5–5 m | 18–36 |
Skytech TK110HW | 32–52 | — | — | 0.3 MP | — | 6–7 | — | — |
JJRC H8D 5.8G FPV RTF RC | 169–175 | UAV: 0.023 | 330 × 330 × 115 | — | 8 | — | — | |
X810 Long Range Uav Sprayer | 4000–6500 | Payload: 10 | 2490 × 1645 × 845 (L.W.H) | — | — | 25–40 | — | — |
Syma X8C | 68.99 | — | 508 × 508 × 165 (L.W.H) | 2 MP HD Camera | — | 5–8 | — | — |
Controller | Noise | Actuator limits | Rise time (s) | Settling time (s) | Overshoot (%) |
---|---|---|---|---|---|
PID | — | — | 0.61 | 0.95 | 4.2 |
PID | Y | Y | 1.28 | Inf | 10.1 |
LQR | — | Y | 1.01 | 1.9 | 2.1 |
LQR | Y | Y | 3.3 | 3.95 | 0 |
Observer | Y | Y | 1.9 | Inf | 34.5 |
A comparison between the proposed controllers.
LQR controllers however work in the state-space and are suited for MIMO control. It assumes full state feedback; that is, all the system’s states are available for the controller to take decisions, even though this might not be a case in reality. Therefore, we designed the observer to deal with this issue. The outputs of the LQR controlled system response with actuator dynamics are shown in Figures 19 and 20. Unlike the PID controller, the LQR handles actuator dynamics inconsequentially. Appropriate waiting matrices were assigned, and the LQR controller matrix was obtained by using the MATLAB
LQR full state feedback response without noise.
LQR with observer response with noise.
From the plots of LQR with observer (Figure 20), it can be seen that the system is in the verge of instability and the noise content of the pitch signal disturbs the velocity severely. The relative stability of the given system can be discussed in terms of the gain margin and phase margin. Based on the Bode plots analysis of the open-loop system (plots not provided for the sake of paper page limits), the differential term in the elevator input to output relationships reduces the phase margin of system considerably. Model errors and disturbance in the pitch rate could easily drive the system to instability. This agrees with the findings in the controller design exercised.
Health assessment and conventional scouting of oil palms on a regular basis, as well as palm census and quantification of the amount of fresh fruit bunches (FFB) for yield monitoring, are labor-intensive tasks that are either ignored in large scale plantations or are carried out manually by the use of labor force. Traditional scouting is not only an ineffective practice but also requires expert knowledge and post-processing lab equipment to provide useful information. Advances in aerospace engineering, control system, and computing have contributed significantly to the improvement of UAV-based remote sensing platforms. This paper discussed some of the potential applications of UAVs for precision agriculture of oil palm plantations. We also highlighted some of the adaptation challenges faced by UAV drones, including platform stability due to the flight dynamics parameters and winds, climate factors and light reflection degrading quality of the acquired images, and regulations and restrictions law by the Federal Aviation Administration. As a response to the needs of small-scale plantation owner for an affordable UAV platform, a fixed-wing Osprey drone was proposed and used in designing an auto-flight control. The aircraft can be externally actuated by controlling the thrust (
Names and specifications of sample multi-rotor and fixed-wing UAV recommended for precision agriculture of oil palm.
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