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Modified Atkins Diet and Low Glycemic Index Treatment for Medication Resistant Epilepsy Current Trends in Ketogenic Diet 2155 9562.S2 007

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  Research ArticleOpen Access Kumada et al., J Neurol Neurophysiol 2013, S2http://dx.doi.org/10.4172/2155-9562.S2-007   Case ReportOpen Access Neurology & Neurophysiology J Neurol Neurophysiol ISSN: 2155-9562 JNN, an open access journal Epilepsy: Current Trends Modified Atkins Diet and Low Glycemic Index Treatment for Medication-Resistant Epilepsy: Current Trends in Ketogenic Diet Tomohiro Kumada*, Tomoko Miyajima, Ikuko Hiejima, Fumihito Nozaki, Anri Hayashi and Tatsuya Fujii Department of Pediatrics, Shiga Medical Center for Children, Shiga, Japan *Corresponding author:  Dr. Kumada, Department of Pediatrics, Shiga Medical Center for Children, Moriyama, Japan, Tel: +81 77 582 6200; Fax: +81 77 582 6304; E-mail: tkumada@mccs.med.shiga-pref.jp Received  March 13, 2013; Accepted  June 13, 2013; Published  June 20, 2013 Citation:  Kumada T, Miyajima T, Hiejima I, Nozaki F, Hayashi A, et al. (2013) Modied Atkins Diet and Low Glycemic Index Treatment for Medication-Resistant Epilepsy: Current Trends in Ketogenic Diet. J Neurol Neurophysiol S2: 007 doi:10.4172/2155-9562.S2-007 Copyright:  © 2013 Kumada T, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the srcinal author and source are credited. Keywords : Ketogenic diet; Modified Atkins diet; Low glycemic index treatment; Epilepsy Introduction Te ketogenic diets (KDs) have been used or the treatment o medication-resistant epilepsy since the 1920s. Te classical KD is a highly restrictive diet with a 3:1-4:1 ketogenic ratio, calculated as the weight o at divided by that o carbohydrates plus protein. Although the classical KD result in at least a 50% reduction in seizure requency in approximately hal o epileptic patients, some patients cannot tolerate the diet over a long period o time because o its restrictiveness. Consequently, the modified Atkins diet (MAD) and the low glycemic index treatment (LGI) that are more liberal and less restrictive than the classical KD, were developed in the 1990-2000s [1,2]. Contrary to the classical KD, these diets can be provided without restriction o calories, protein and fluid intake, and calculation o ketogenic ratio is not necessary. Figure 1 shows the distribution o major nutrients in calories in each diet [1,2]. MAD and LGI have a similar composition pattern and the percentage o at is less than in KD. Tese new KDs weigh greater importance in having a stable blood glucose level than the production o ketone bodies.Because the KDs including MAD and LGI are the therapy that the patients and parents must prepare by themselves, the menus o the KDs are greatly affected by their ood culture. Tus, the practical menus o these KDs differ among countries based on various local ood cultures although the concepts o these KDs are common globally. For example, Japanese patients and parents cannot cook daily KDs menus by reerring to the textbooks on the KDs in Western countries because the available oods and the tastes are different between Japan and Western countries. Tereore, we have designed the MAD and LGI menus which Japanese patients and parents can easily prepare and resemble to normal Japanese ethnic menus.In this paper, we describe the history o development o the KDs, their methods and the evidence o clinical efficacy rom the previous literatures. In particular, we present how Japanese patients and parents can cook the MAD and LGI menus using Japanese ethnic oods concretely in the section o ‘dietary concept, compositon, and menu’ o each diet. We also describe our own clinical experience in each o these diets, and discuss which o these KDs (MAD or LGI) should be selected in different patients. History of the KDs from fasting to the LGI An overview o the history o the KDs shows that the ocus has changed rom a diet that produces ketone bodies efficiently, which mimics asting, to one that is palatable and can thereore be ollowed with high compliance. From the period o Hippocrates, it has been known that seizures can be treated by asting [3]. Te KD protocols consisting o high at and low carbohydrate were designed to mimic the metabolic effect o asting. In 1921, Geyelin reported to the American Medical Association that the beneficial effect o asting continued even afer the ast was broken. Ten, Wilder theorized that the benefit o the diet depends on the ketonemia observed by Geyelin [3,4]. He showed that ketosis occurred when the ratio o atty acids to glucose was >2:1. From this theory, the classical KD was developed and it was widely used in the treatment o epilepsy. Huttenlocher developed a medium chain triglyceride diet in an attempt to make the classical KD more palatable. With the advancement o the pharmacotherapy or epilepsy, however, the KD treatment has gradually become replaced by antiepileptic drugs, particularly afer the introduction o carbamazepine and valproic acid in the 1970-80s.A revival boom o the KDs occurred in the 1990s, starting with an NBC Dateline report in 1994. Soon afer, the television movie, “First, Do No Harm”, starring Meryl Streep, which was a dramatization o the lie o a patient with epilepsy, turned the public’s eye to the diet in 1997. In the last decade, the KDs became popular globally; the 1 st  international symposium on dietary treatments or epilepsy and other neurological disorders was held in 2008, and the international consensus recommendation was published in Epilepsia  in 2009 [5]. Abstract Compared to the classical ketogenic diet (KD), the modied Atkins diet (MAD) and the low glycemic index treatment (LGIT) are more liberal and less restrictive diet therapies for the treatment of medication-resistant epilepsy. The MAD was rst reported by Kossoff et al. in 2003, and gained global popularity with sufcient evidence in its efcacy reported recently in a controlled study. The LGIT was rst reported by Pfeifer et al. in 2005, and its use has also become widespread. We reviewed the efcacy of both diet therapies in the treatment of medication-resistant epilepsy based on the evidence from previous literatures and our own clinical experience. From our experience, the LGIT was more liberal, tolerable, and dietetically balanced than the MAD. To nd out which of these diets is most appropriate in different epilepsies and different patients, future controlled comparative studies on the efcacy, tolerability, and dietetic advantages between the MAD and the LGIT are necessary.  Page 2 of 6 Citation: Kumada T, Miyajima T, Hiejima I, Nozaki F, Hayashi A, et al. (2013) Modied Atkins Diet and Low Glycemic Index Treatment for Medication-Resistant Epilepsy: Current Trends in Ketogenic Diet . J Neurol Neurophysiol S2: 007 doi:10.4172/2155-9562.S2-007 J Neurol Neurophysiol ISSN: 2155-9562 JNN, an open access journal Epilepsy: Current Trends Meanwhile, Kossoff rom Johns Hopkins University Hospital designed and reported on a new and more liberal KD called ‘MAD’ in 2003 [6]. Since then, numerous articles on MAD have been published rom all over the world, including USA [7,8], Denmark [9,10], France [11], Belgium [12], Korea [13,14], India [15], Iran [16], and Japan [17]. Separately, in 2005, Peier rom Massachusetts General Hospital developed and reported on an alternative ketogenic diet, ‘LGI’, which was more palatable than the MAD [18]. Te diet has also gained a widespread attention. Currently, the MAD and the LGI are the main KDs used in therapy especially in adolescent and adult patients [19]. Te MAD Dietary concept, composition and menu Te MAD was developed at Johns Hopkins Hospital to create a KD that was more liberal and less restrictive than the classical KD or children who were reluctant to ollow the classical KD due to its restrictiveness [1]. Dr. Atkins srcinally developed the diet in the 1970s as a method or weight reduction or people suffering rom obesity. Tis diet was modified so that the at intake was increased while the carbohydrate restriction was maintained the same as in the “introduction phase” o the srcinal method. Te carbohydrate content o the diet is restricted to 10 g per day at the initiation o the MAD, and is subsequently maintained at 10-30 g per day. Calories, protein and fluids are not restricted. As shown in (Figure 1), the proportion o calories rom at is decreased in the MAD compared to the classical KD. Te amount o calories remained rom the decrease in at are assigned to protein so that the ketogenic ratio resulted in 1:1 to 2:1 in the MAD diet. Figure 2a and 2b shows an example o a lunch menu o the MAD in our hospital. Te content o carbohydrates, protein, and at in this menu was 2.5 g, 26.8 g, and 42.8 g respectively, and the ketogenic ratio was 1.46:1, which was lower than that o the classical KD, 3:1 to 4:1. Evidence of efficacy based on previous literatures More than 50 articles on the use o MAD or medication-resistant epilepsy have been published since Kossoff et al. first reported on the diet in 2003, and there is accumulating evidence or its efficacy [5]. Auvin reviewed 7 prospective and 2 retrospective reports, and summarized the efficacy o MAD as ollows [20]; the responder rate (the proportion o patients with >50% seizure reduction) was 51/87 (59%) afer 1 month, 73/152 (48%) afer 3 months, and 46/119 (39%) afer 6 months o MAD therapy. Chen et al. investigated the long-term efficacy o the MAD and reported that the responder rate was 64/87 (74%) afer 1 month, 36/54 (67%) afer 6 months, 28/35 (80%) afer 12 months, and 8/16 (50%) afer 24 months in intent-to-treat analysis [21]. Recently, a randomized controlled trial o the use o MAD or the treatment o medication-resistant childhood epilepsy published by Sharma et al. [22], showed that the proportion o patients with >90% seizure reduction (30% vs. 7.7%, p=0.005) and that with>50% seizure reduction (52% vs. 11.5%, p<0.001) was significantly higher in the MAD group than in the control group afer 3 months. A number o published reports have shown the efficacy o the MAD in specific epilepsy syndromes and underlying diseases including inantile spasms [15], absence epilepsy [23], juvenile myoclonic epilepsy [24], Sturge-Weber syndrome [25], and nonconvulsive status epilepticus [26]. Our experience In our group, we have been treating medication-resistant epilepsy with the MAD since 2007. Upon admission, the MAD was initiated with a restriction o the carbohydrate content o the diet to10 g per day, and the total calorie content was adjusted to match the patients’ usual caloric intake beore the diet. Afer 3 to 4 weeks on the diet, we let the parents decide whether or not to continue the diet. We then ollow the patients afer discharge every 1-3 months at the out-patient clinic. In the current report, we summarized data rom 16 patients who started the MAD in our hospital. able 1 shows the profile and short-term efficacy and tolerability afer 3 months on the diet in all o the patients, including 10 patients reported elsewhere [17]. Eight patients could not continue the diet or more than 3 months. Four o them, Regular DietClassical KDLGITMAD Figure 1: Percentage of carbohydrate, fat, and protein in the regular diet, the classical KD, the MAD, and the LGIT.  Page 3 of 6 Citation: Kumada T, Miyajima T, Hiejima I, Nozaki F, Hayashi A, et al. (2013) Modied Atkins Diet and Low Glycemic Index Treatment for Medication-Resistant Epilepsy: Current Trends in Ketogenic Diet . J Neurol Neurophysiol S2: 007 doi:10.4172/2155-9562.S2-007 J Neurol Neurophysiol ISSN: 2155-9562 JNN, an open access journal Epilepsy: Current Trends including one who was inected with viral gastroenteritis, reused the menus. In the remaining 4 patients, their amilies gave up preparing the MAD afer discharge. Excluding these drop-outs, the efficacy at 3 months was as ollows: 3 individuals were excellent responders (seizure-ree), 1 was a good responder (>50% seizure reduction), and the diet was not efficacious in the remaining 4. Te values o serum beta-hydroxybutyrate were elevated over 2000umol/L at 3 months on the diet in all cases investigated. Te long-term efficacy o the MAD in our patients is shown in Figure 3. Te responder rate was 4/8 (50%) afer 3 months, 3/6 (50%) afer 6 months, 3/4 (75%) afer 12 months, and 2/4 (50%) afer 24 months on the diet. All o 4 patients who completed 24 months o the diet discontinued the diet aferwards. One patient (case-2) o those who achieved seizure control at the 24 months has been seizure-ree since then, although the other patient (case-3) suffered a relapse o seizures soon afer the diet was stopped. Tere were no side effects on the laboratory examinations during the course o the diet except serum total-cholesterol which were slightly elevated (270-300 mg/dl) in some patients. Tere were no patients who experienced weight loss or ailure o appropriate weight gain during the diet. Severe side effects, which led to an interruption o the MAD occurred in 3 patients: generalized atigue with severe acidosis (pH 7.20 on blood gas analysis) on the third day o the diet (case-2). Generalized atigue with unknown cause within 1 week on the diet (case-9), and ainting with hypoglycemia due to reusal o ood intake afer one month on the diet (case-16). Although case-9 and -16 gave up the restart o the MAD, case-2 could resume the MAD ten days later. Our results suggest that even the MAD has potentially severe lie-threatening side effects, especially in the early period rom the start o the diet, although many authors have emphasized that the MAD can be saely introduced without hospital admission in contrast to the classical KD [1]. Te Low Glycemic Index reatment (LGI) Dietary concept, composition and menu Te glycemic index (GI), designed by Jenkins in 1981 [2], is an indicator o the degree o the increase o blood glucose levels by a specific ood as compared to that o a standard ood. Low GI oods have since been used or the treatment o diabetes mellitus and obesity. In 2005, Peier et al. rom Massachusetts General Hospital first reported on an alternative ketogenic diet, ‘LGI’ or the purpose o maintaining compliance to diet therapy [18]. Tis diet allows a more liberal daily intake o carbohydrates (40-60 g per day) than the other KDs, on condition that the GI o carbohydrates is restricted to less than 50 relative to glucose. In the LGI, a typical proportions o calories are as ollows; 60-65% rom at, 20-30% rom protein, and 10-15% rom carbohydrates (Figure 1). Calories and fluids are not restricted. As a result, the diet is a more palatable and less rigid KD (ketogenic ratio is almost 1:1). Te oods do not need to be weighed since the amount is based on portion sizes, which are based on diabetic exchanges. Te GI values o oods available in Western countries can be ound in the literature [27]. In addition to this report, we used the list o the GI values o Japanese oods prescribed in our previous report [28]. Japanese ethnic oods such as udon (flour noodle), soba (buckwheet noodle), and unpolished Japonica rice mixed with various supplements such as natto  (ermented soybeans) and grated   yam are all available in the LGI.   Figure 2c shows an example o a lunch menu or the LGI used in our hospital, in which the total daily calorie intake is 1600 kcal. Te carbohydrate used in the lunch was unpolished Japonica rice mixed with natto . Te GI value o the unpolished rice is lower than that o polished rice because it has more fiber than its polished counterpart, which can delay the absorption o glucose rom the intestine and decrease the speed at which blood glucose increases. Moreover, when mixed with natto , the rate o glucose absorption was reduced, and the GI value o unpolished rice decreases urther to ewer than 50 relative to glucose. Te content o carbohydrates, protein, and at in Figure 1c was 22.2 g, 19.3 g, and 39.5 g respectively, and the ketogenic ratio was 0.95:1, which is lower than that o the classical KD and the MAD. Evidence of efficacy based on previous literatures Te LGI was first reported to be effective or the treatment o medication-resistant epilepsy at Massachusetts General Hospital [18]. In their recent report, the responder rate was 42%, 50% ,54% 64%, and 66% at 1, 3, 6, 9 and 12 months afer treatment, respectively in intent-to-treat analysis [29]. Coppola et al. rom Italy showed that 8 o 15 a. Regular diet  b. c. MADLGIT proteincarbohydrateketogenic ratio24.1 g77.6 g0.12:1fatTotal calorie11.8 g520 kcalproteincarbohydrateketogenic ratio26.8 g 2.5 g1.46:1fatTotal calorie42.8 g517 kcalproteincarbohydrateketogenic ratio19.3 g22.2 g0.95:1fatTotal calorie39.5 g520 kcal Figure 2: Examples of a lunch menu for the regular diet, the MAD, and the LGIT Each style of lunch menu was provided to case-13 at our hospital. A regular diet which she ate before the start of the MAD at 11 years of age. The lunch consisted of polished rice, boiled mackerel, salad with bean sprouts, nimono  (boiled dish), and banana. The ketogenic ratio was 0.12:1. This is an example of a diet usually preferred by Japanese. b. A MAD menu which she ate during MAD therapy at 11 years of age. The lunch consisted of sauteed chicken with green beans and bacon, scrambled eggs with mayonnaise, and miso  (soybean paste) soup. The ketogenic ratio was 1.46:1. c. A LGIT menu which she ate during the LGIT at 13 years of age. The lunch consisted of unpolished rice with natto , pork beans, tuna salad, miso  soup, and sauteed chicken. The ketogenic ratio was 0.95:1.  Page 4 of 6 Citation: Kumada T, Miyajima T, Hiejima I, Nozaki F, Hayashi A, et al. (2013) Modied Atkins Diet and Low Glycemic Index Treatment for Medication-Resistant Epilepsy: Current Trends in Ketogenic Diet . J Neurol Neurophysiol S2: 007 doi:10.4172/2155-9562.S2-007 J Neurol Neurophysiol ISSN: 2155-9562 JNN, an open access journal Epilepsy: Current Trends patients (53%) with the LGI achieved >50% seizure reduction in the first report published outside o Massachusetts General Hospital [30]. Recently, successul treatments with the LGI or seizures associated with tuberous sclerosis complex [31], Angelman syndrome [32], and mitochondrial disorder [33] have also been reported. However, no controlled studies on the efficacy o the LGI or the treatment o medication-resistant epilepsy are available. o qualiy the evidence or the LGI, randomized controlled studies are necessary. Our experience We first introduced the LGI to case-13 in able 1 because she had reused to comply with the   MAD only 2 weeks afer the diet therapy even though her seizures remitted with the MAD. She continued to tolerate the LGI or over 1 year and achieved >50% seizure reduction. Her detailed clinical course with this diet therapy will be published elsewhere [28]. We have tried the LGI in only 3 patients and no reports other than ours are available in Japan so ar. It seems, thereore, that the LGI has not yet become a popular therapy or medication-resistant epilepsy in Japan. However, we assume that this diet will gain popularity in this country where the rice is a staple ood; rice is acceptable with this diet therapy although only unpolished and a small amount o rice were permitted. Which diet should we use, the MAD or the LGI? Several reports in the literature compared the efficacy o the classical KD and the MAD: wo articles reported a tendency or a higher responder rate with the classical KD than the MAD afer 6 months (7/17 vs. 2/10, p=0.41 in Porta et al. [11], 30/50 vs. 13/33, p=0.06 in Miranda et al. [34]), although the differences were not significant. Kossoff et al. reported that patients with Doose syndrome achieved more seizure control by switching rom the MAD to the classical KD [35]. In addition, Auvin insisted that the classical KD, not the MAD 00%90%80%70%60%50%40%30%20%10%0%1 month 3 month 6 months 12 months 24 months disconnued poorgood excellent Figure 3: Percent of patients with excellent response (seizure-free), good response (>50% seizure reduction), poor response (<50% seizure reduction) on LGIT, and discontinued at each follow up interval. Case/sexAge at theUnderlyingEpilepsySeizureSeizure  Efcacy Reasons ofbeta-hydroxy-start of MADdisease  classication phenotypefrequencyat 3 monthsdiscontinuationbutyrate at 3 months 1/Male1y6mleukodystrophy SLRE Complex Partial Weekly Discontinued Reject By Patient -2/Female1y6mTrisomy 21ISSpasmsDailyExcellent 4929 umol/L 3/Male1y11mISSpasms, TonicDailyExcellent 3986 umol/L 4/Male2y2mISSpasms, TonicDailyUnchanged 5470 umol/L 5/Female3yDooseMAS, MyoclonicDailyDiscontinued Reject By Family -6/Female3yISSpasms, TonicDailyUnchangednot done7/Female3yISSpasms, TonicDailyUnchangednot done8/Male3yISSpasms, TonicDailyUnchanged 6174 umol/L 9/Female3ytuberous sclerosis LGS Tonic, Atypical AbsenceDailyDiscontinued Reject By Patient -10/Female5yband heterotopia unclassiedNCSE, Gtcs, Drop DailyExcellent 2376 umol/L 11/Female5y SLRE NCSE, Tonic, HypermotorDaily Good2795 umol/L 12/Male7y SLRE Tonic Weekly Discontinued Reject By Family -13/Female11ytuberous sclerosis LGS Tonic, Atypical AbsenceDailyDiscontinued Reject By Patient -14/Female17ytuberous sclerosis LGS Tonic, Atypical AbsenceDailyDiscontinued Reject By Family -15/Female29y15q inv dup syndrome SLRE DailyDiscontinued Reject By Family -16/Female32y SLREComplex Partial, GtcsWeekly Discontinued Reject By Patient - Table 1:  Proles of patients who started the MAD in our hospital and the short-term efcacy and tolerability after 3 months on the diet Abbreviations: SLRE, symptomatic localization-related epilepsy; IS, infantile spasms; LGS, Lennox-Gastaut syndrome; Doose, Doose syndrome; NCSE, nonconvulsive status epilepticus; GTCs, generalized tonic clonic seizure; excellent, seizure-free; good, >50% seizure reduction; unchanged; <50% seizure reduction.
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