ICAN: Infant, Child, & Adolescent Nutrition. Ketogenic Diet Patients Lipid Profiles Improved With KetoCal 4:1 Liquid
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1 580362CANXXX / Infant, Child, & Adolescent NutritionMONTH MONTH XXXXvol. X no. XInfant, Child, & Adolescent Nutrition research-articlexxxx Evidence-Based Practice Reports Ketogenic Diet Patients Lipid Profiles Improved With KetoCal 4:1 Liquid A Case Series Sue A. Groveman, MS, RD, LDN, Cagla Fenton, RD, LDN, Rebecca Randall, MS, RD, LDN, Claire M. Chee, RN, BS, and A. G. Christina Bergqvist, MD Abstract: Objective. The ketogenic diet (KD) can result in hyperlipidemias. We report improvements in the lipid profiles of 3 children who were switched from KetoCal 4:1 powder (formulation prior to fall 2013) to KetoCal 4:1 Liquid formula. Compared with the KetoCal 4:1 powder formulation prior to fall 2013, KetoCal 4:1 Liquid has no transfatty acids, reduced saturated fatty acids, added omega-3 fatty acids, and added fiber. Methods. A retrospective chart review revealed 3 patients in our KD program with elevated lipid profiles while receiving 100% of their nutritional needs from KetoCal 4:1 powder. The patients were switched to KetoCal 4:1 Liquid and treated for >3 months. Fasting lipid profiles were obtained before and 2 to 3 months after the formula switch. All patients were on 4:1 ratio KD formula. Results. After changing formulas, the lipid profiles of all 3 patients improved. Mean total cholesterol, triglycerides, and low-density lipoprotein were reduced by 29%, 33%, and 58%, respectively. High-density lipoprotein increased by 10% on average. Conclusion. A decrease in lipid levels was observed with the transition to KetoCal 4:1 Liquid after an average of 2.1 months. Changes in dietary fat profile (including addition of omega-3 fatty acids) and the addition of fiber in enteral formulas can positively affect lipid profiles of tube-fed KD patients. Keywords: ketogenic diet; lipids; enteral formula; epilepsy; cholesterol; hyperlipidemia; triglycerides The ketogenic diet (KD) is a dietary intervention used for children with treatment-resistant epilepsy and for certain metabolic disorders such as pyruvate dehydrogenase deficiency and glucose transporter type-1 protein deficiency. In the case of these metabolic disorders, it is the primary treatment available and will likely be a long-term treatment. The KD can be effective in reducing seizures when antiepileptic drugs fail. Short-term seizure control is well documented, and in general two thirds of children have a greater than 50% reduction in seizures and up to 20% may become seizure-free. 1,2 Neal et al 3 found, in a randomized control study of 145 children, that KD patients had a significantly lower percentage of seizures compared with controls (62.0% vs 136.9%). Children who are fed via gastrostomy tube may achieve similar The KD can be administered in many forms: as oral meals, formula for infants, tube feedings, or as total parenteral nutrition. effectiveness. Twelve KD patients fed via gastrostomy tube were studied by Hosain et al, 4 who found that their seizures were reduced by >60%. In this diet, 90% of the calories come from fat, 7% to 8% from protein, and 2% to 3% from carbohydrates. Due to the high percentage of fat in the diet, a side effect of the KD often encountered is elevated lipid levels. Significantly DOI: / From the Department of Clinical Nutrition (SAG, CF, RR) and Division of Neurology (CMC, AGCB), The Children s Hospital of Philadelphia, Philadelphia, Pennsylvania. Address correspondence to Sue A Groveman, MS, RD, LDN, Department of Clinical Nutrition, The Children s Hospital of Philadelphia, 34th Street and Civic Center Boulevard, Suite 9NW-82, Philadelphia, PA 19104; grovemans@ .chop.edu. For reprints and permissions queries, please visit SAGE s Web site at Copyright 2015 The Author(s) 157
2 June 2015 Table 1. Formula Products Nutrition Comparison a. Nutrient Content increased total cholesterol (TC), low-density lipoprotein (LDL), and triglycerides (TG) combined with significantly decreased high-density lipoprotein (HDL) have been reported in up to 50% of patients after starting the KD. 5,6 Hyperlipidemia has been shown to occur within days of KD initiation. 7 Kang et al 8 reported significantly elevated cholesterol in 14.7% of patients and significantly elevated triglycerides in 27.1% of patients. Hyperlipidemia is not a reason to discontinue the KD. Lipids should be monitored every 3 months. 9 Nutrition counseling can be beneficial for those patients who eat by mouth. It has been shown that modifying the type of dietary fat (increased polyunsaturated fats [PUFA] and reduced saturated fats [SFA]) ingested can improve the lipid profile. 10 The KD can be administered in many forms: as oral meals, formula for infants, tube feedings, or as total parenteral KetoCal 4:1 KetoCal 4:1 Powder b Liquid % Calories fat Total fat (g) c % Polyunsaturated fat % Monounsaturated fat % Saturated fat % Trans fat 35 0 Total protein (g) c Total carbohydrates (g) c ARA (mg) c DHA (mg) c Total soluble and insoluble fiber (g) c Sweetener Aspartame Sucralose a Personal Communication from Manufacturer b Formulation prior to fall c Per 100 calories. nutrition. Due to concurrent developmental delays, feeding difficulties, and impaired neurological status, many of the children on the KD are fed formula via a feeding tube. At The Children s Hospital of Philadelphia, approximately one third of the patients in the KD program are fed with a gastrostomy or jejunostomy tube. Similar numbers have been published at other institutions. 11 There are currently only a few options for children who need commercially available KD enteral formulas. Prior to May 2010, KetoCal 4:1 powder was one of the only choices for formula. The formulation of this product (prior to fall 2013) included 36% trans-fatty acids (TFA) and 23% SFA (Table 1). In May 2010, Nutricia North America introduced a liquid version of the KetoCal 4:1 powder with an improved lipid profile and the addition of omega-3 fatty acids and fiber. As shown in Table 1, the TFA were completely removed from the formulation and the SFA was reduced to 15% in KetoCal 4:1 Liquid. The purpose of this case series is to describe how changes in the KetoCal formula affected blood lipid levels in 3 patients who were 100% tube-fed. Methods A retrospective chart review was performed. Inclusion criteria were the following: 100% tube-fed and switched from KetoCal 4:1 powder (formulation prior to fall 2013) to KetoCal 4:1 Liquid after a minimum of 3 months on each treatment. Fasting lipid profiles were obtained before and on average every 3 months after the formula switch. All patients were on 4:1 KD ratio (the grams of fat to the grams of protein and carbohydrates combined). All patients had been started on the KD as per our gradual KD initiation protocol previously published. 12 Results The retrospective chart review revealed 3 patients (2 females, 1 male) ranging from 2 to 7 years of age at the time of KD initiation (Table 2). The duration of time on the KD before switching to KetoCal 4:1 Liquid ranged from 9 months to 57 months. Two of the patients were on a 4:1 KD ratio, and 1 patient was on a 4.25:1 ratio. Prior to switching formulas, all 3 had elevated TC, LDL, and TG with low HDL levels. After changing formulas, the lipid profiles improved (Table 3). Mean TC, TG, and LDL were reduced by 29%, 33%, and 58%, respectively. HDL increased by 10% on average. During this time period, the 3 patients increased in weight and body mass index. One of the patients had a small increase (8%) in calories; the other 2 patients had no changes in calories. Discussion The KD is an effective treatment for epilepsy but can have a common side 158
3 Table 2. Patient Demographic/Diet Information. Gender Age at KD Initiation (Years) effect of hyperlipidemia. The KD at The Children s Hospital of Philadelphia typically consists of a 2-year treatment with 1 year of weaning off the diet. 13 However, children whose seizures recur or worsen with the weaning may choose to stay on the KD longer. At our center, we have patients who have remained on the KD for 15 years, which puts them at an even greater risk for side effects. Side effects from persistent long-term hyperlipidemia include coronary artery disease, pancreatitis, fatty liver, angina, hypertension, and stroke. Hyperlipidemia as a child can lead to health issues later in life. For example, elevated lipids can foreshadow the beginnings of cardiovascular disease in young adults. Berenson et al 14 performed autopsies on 204 young people (2-39 years of age) and compared the signs of atherosclerosis (fatty streaks and fibrous plaques) with cardiovascular risk factors (body mass index, lipid levels, blood pressure, etc). It was established that the lipid levels in young people were strongly associated with the degree of atherosclerosis. The effect of long-term use of the KD on coronary artery disease has not been established, and the hyperlipidemia that often occurs can be managed by manipulating the types of fats used. Previously, we found that changing fat composition of food by mouth can positively affect lipid profiles in the children treated with the KD. 10 Now, we have shown in 3 cases that changing enteral formula can affect the lipid KD Ratio at Time of Switch to KetoCal 4:1 Liquid Length of Time on KD at Time of Switch to KetoCal 4:1 Liquid (Months) Patient 1 Male 2.6 4:1 23 Patient 2 Female 7.3 4:1 57 Patient 3 Female :1 9 profiles of children on tube feeds in as short a period as 3 months. During this time period, all 3 patients had no decreases in weight, body mass index, or caloric intake. These variables did not therefore contribute to the improved lipid profiles. In a 1500 calorie diet of KetoCal 4:1 powder, there was a substantial amount of TFA (53.5 g) and SFA (34.2 g) per day. The American Heart Association recommends limiting TFA to <1% of total calories (1.7 g for 1500 calories) and SFA to <7% (11.7 g for 1500 calories). 15 Although the KD is high in dietary fat, it does not need to be high in TFA or SFA. TFA have been shown to be correlated to elevated lipid profiles and increased risk of myocardial infarction and coronary heart disease as well as insulin resistance, systemic inflammation, and endothelial dysfunction. 16,17 TFA have also been linked with harming vascular function. 18 In a recent review, Hooper et al 19 showed that decreasing dietary SFA reduces risk of cardiovascular incidents by 14%. The healthier dietary fats are the PUFA and monounsaturated fat (MUFA), which have been linked to improved lipid profiles and lower cardiac disease risk factors. 20,21 Medium-chain triglycerides, a type of saturated fat, have the potential to reduce triglycerides. 22 The omega-3 fatty acid docosahexaenoic acid (DHA) was added to the KetoCal liquid. Two to 4 g/day of DHA has been found to reduce TGs by 25% to 35%. 23 The amount of DHA in the patient s formula ranged from 0.24 to 0.48 g/day. This amount of omega-3 fatty acids could have minimally contributed to reducing the patient s triglycerides. The addition of fiber in the liquid formulation of KetoCal may also have influenced the lipid profiles. A metaanalysis by Pereira et al 24 found that for every 10 g/day increment in total dietary fiber, there was a 14% reduction in risk of coronary events. Each gram of water-soluble fiber from psyllium is known to reduce total and LDL cholesterol levels by 1.08 mg/dl and 1.12 mg/dl, respectively. 25 Fiber has not been found to influence HDL or triglycerides. 26 The amount of fiber in the patient s daily feeding regimen ranged from 5.1 g/day to 10.4 g/day. This may have also been a small contributor to the reduction in cholesterol that we found in our patients. We have described 3 cases where even in a diet of 90% dietary fat, switching the type of fat can meaningfully influence lipid profiles. In our case series of 3 patients, switching to formula with no TFA, reduced SFA, increased PUFA/ MUFA, added fiber, and added DHA improved the lipid profiles of all 3 patients (Table 3). The quantities of DHA and fiber added to the formula may have minimally affected the lipid profiles, but it is more likely that the changes were primarily due to the absence of TFA and reduction in SFA. After the change in formula, the TC and LDL fell into the borderline high category for all 3 patients, and for TG, 2 patients were in the borderline high category while 1 patient was just slightly above (Tables 3 and 4). Previously, the KD was viewed as more of a short-term (1-2 years) treatment and side effects of hyperlipidemia were not considered to be of concern. Now the KD is increasingly being used for longer periods of time. Many children who are tube-fed remain on the KD for many years (in some cases more than a decade), requiring formulas with a healthy fat composition. KetoCal 4:1 powder with an improved fat composition was released fall This may help improve lipid profiles of those patients remaining on KetoCal 4:1 159
4 June 2015 Table 3. Mean Results of Lipid Levels in Patients Switched to KetoCal 4:1 Liquid. Total Cholesterol LDL Cholesterol HDL Cholesterol Triglycerides Baseline Post Baseline Post Baseline Post Baseline Post Patient Patient Patient Mean ± SD 257 ± ± ± ± 5 44 ± 1 48 ± ± ± 17 Mean % change 29% 33% 10% 58% Abbreviations: LDL, low-density lipoprotein; HDL, high-density lipoprotein. Table 4. Acceptable Lipid Levels for Children 27. Category Low Acceptable Borderline-High High Total cholesterol < LDL cholesterol < Triglycerides (0-9 years) < HDL cholesterol <40 > Abbreviations: LDL, low-density lipoprotein; HDL, high-density lipoprotein. powder. This will also be an improvement for those families that use KetoCal 4:1 powder in cooking. Conclusion This case series describes 3 patients on the KD who received 100% of their estimated needs from KetoCal 4:1 powder formula (formulation prior to fall 2013). For these patients, KetoCal 4:1 Liquid successfully improved their lipid profiles in an average of 3 months. Clinicians could consider transitioning their patients currently on formula regimens with high levels of TFA or SFA to formula with increased PUFA and MUFA. A study with a larger sample size, possibly using other formulas or blenderized feedings, and longer follow-up is needed to assess the long-term outcomes including the various effects of the KD on cardiovascular health. Author Note The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/ or publication of this article. The author(s) received no financial support for the research, authorship, and/or publication of this article. References 1. Henderson CB, Filloux FM, Alder SC, Lyon JL, Caplin DA. Efficacy of the ketogenic diet as a treatment option for epilepsy: meta-analysis. J Child Neurol. 2006;21: Lefevre F, Aronson N. Ketogenic diet for the treatment of refractory epilepsy in children: a systematic review of efficacy. Pediatrics. 2000;105:E Neal EG, Chaffe H, Schwartz RH, et al. The ketogenic diet for the treatment of childhood epilepsy: a randomised controlled trial. Lancet Neurol. 2008;7: Hosain SA, La Vega-Talbott M, Solomon GE. Ketogenic diet in pediatric epilepsy patients with gastrostomy feeding. Pediatr Neurol. 2005;32: Kwiterovich PO Jr, Vining EP, Pyzik P, Skolasky R Jr, Freeman JM. Effect of a high-fat ketogenic diet on plasma levels of lipids, lipoproteins, and apolipoproteins in children. JAMA. 2003;290: Chesney D, Brouhard BH, Wyllie E, Powaski K. Biochemical abnormalities of the ketogenic diet in children. Clin Pediatr (Phila). 1999;38: Dekaban AS. Plasma lipids in epileptic children treated with the high fat diet. Arch Neurol. 1966;15:
5 8. Kang HC, Chung DE, Kim DW, Kim HD. Early- and late-onset complications of the ketogenic diet for intractable epilepsy. Epilepsia. 2004;45: Bergqvist AG. Long-term monitoring of the ketogenic diet: do s and don ts. Epilepsy Res. 2012;100: Fenton C, Chee C, Bergqvist A. Manipulation of types of fats and cholesterol intake can successfully improve the lipid profile while maintaining the efficacy of the ketogenic diet. Infant Child Adolesc Nutr. 2009;2: Kossoff EH, McGrogan JR, Freeman JM. Benefits of an all-liquid ketogenic diet. Epilepsia. 2004;45: Bergqvist AG, Schall JI, Gallagher PR, Cnaan A, Stallings VA. Fasting versus gradual initiation of the ketogenic diet: a prospective, randomized clinical trial of efficacy. Epilepsia. 2005;46: Kossoff EH, Zupec-Kania BA, Amark PE, et al. Optimal clinical management of children receiving the ketogenic diet: recommendations of the International Ketogenic Diet Study Group. Epilepsia. 2009;50: Berenson GS, Srinivasan SR, Bao W, Newman WP 3rd, Tracy RE, Wattigney WA. Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. The Bogalusa Heart Study. N Engl J Med. 1998;338: Lichtenstein AH, Appel LJ, Brands M, et al. Diet and lifestyle recommendations revision 2006: a scientific statement from the American Heart Association Nutrition Committee. Circulation. 2006;114: Mozaffarian D, Aro A, Willett WC. Health effects of trans-fatty acids: experimental and observational evidence. Eur J Clin Nutr. 2009;63(suppl 2):S5-S Wallace SK, Mozaffarian D. Trans-fatty acids and nonlipid risk factors. Curr Atheroscler Rep. 2009;11: Nestel P. Trans fatty acids: are its cardiovascular risks fully appreciated? Clin Ther. 2014;36: Hooper L, Summerbell CD, Thompson R, et al. Reduced or modified dietary fat for preventing cardiovascular disease. Cochrane Database Syst Rev. 2012;(5):CD Michas G, Micha R, Zampelas A. Dietary fats and cardiovascular disease: putting together the pieces of a complicated puzzle. Atherosclerosis. 2014;234: Hu FB, Manson JE, Willett WC. Types of dietary fat and risk of coronary heart disease: a critical review. J Am Coll Nutr. 2001;20: Hauenschild A, Bretzel RG, Schnell-Kretschmer H, Kloer HU, Hardt PD, Ewald N. Successful treatment of severe hypertriglyceridemia with a formula diet rich in omega-3 fatty acids and medium-chain triglycerides. Ann Nutr Metab. 2010;56: Harris WS, Ginsberg HN, Arunakul N, et al. Safety and efficacy of Omacor in severe hypertriglyceridemia. J Cardiovasc Risk. 1997;4: Pereira MA, O Reilly E, Augustsson K, et al. Dietary fiber and risk of coronary heart disease: a pooled analysis of cohort studies. Arch Intern Med. 2004;164: Brown L, Rosner B, Willett WW, Sacks FM. Cholesterol-lowering effects of dietary fiber: a meta-analysis. Am J Clin Nutr. 1999;69: Theuwissen E, Mensink RP. Water-soluble dietary fibers and cardiovascular disease. Physiol Behav. 2008;94: Expert panel on integrated guidelines for cardiovascular health and risk reduction in children and adolescents: summary report. Pediatrics. 2011;128(suppl 5):S213-S
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