the vagus nerve—a common route for epilepsy therapies?

1
For personal use. Only reproduce with permission from Elsevier Ltd. 518 Reflection & Reaction Neurology Vol 3 September 2004 http://neurology.thelancet.com The vagus nerve—a common route for epilepsy therapies? One mechanism not covered in the recent review by Eric Kossoff 1 is that the ketogenic diet (and other treatments for epilepsy) may act indirectly on the brain via the subabdominal left cervical-brain- stem–vagus-nerve route. Information about physiological factors (eg, appetite) travels along this nerve between the brain and visceral organs, such as the liver and intestines. External electrical stimulation of the left cervical vagus nerve is an established treatment for epilepsy; 2 antiepileptic drugs or dietary therapies may therefore exert their effect via internal stimulation of this route. Diets rich in fatty acids and those that mimic fasting, such as the ketogenic diet and the Atkin’s diet, have appetite-suppressing effects. Recent studies have shown that the fatty-acid- like molecule oleoylethanolamide suppresses appetite through a mechanism that is dependent on an intact vagus nerve. 3 This effect of oleoylethanolamide is also dependent on the presence of functional peroxisome proliferator activated receptor alpha (PPAR), probably located in the liver or the intestine in cells adjacent to vagus-nerve afferents. 3 PPAR has been implicated in the metabolic effects of ketogenic diet or fasting on processes in the liver and the brain, 4 and, indeed, oleoylethanolamide is a ligand for PPAR. Thus, it is proposed that the appetite suppressing effects of oleoylethanolamide are mediated via activation of hepatic and intestinal PPAR; these effects cause changes in cell state that stimulate the neighbouring vagus-nerve afferents. Interpretation of such vagus-nerve signals in the hypothalamus results in appetite suppression via behavioural modifications. In addition to oleoylethanolamide, PPAR has an unusually broad range of ligands, including many fatty acids 5 abundant in the ketogenic diet. Moreover, fatty-acid-like drugs, such as valproic acid and several valproic-acid analogues, activate PPAR. 6 There is also a relation between potency of PPAR activation and antiseizure efficacy. 5 This finding is particularly intriguing because other antiepileptic drugs may already be exploiting the internal route of vagus-nerve stimulation. Despite poor access to the brain, the hormone epinephrine may exert an antiseizure effect via stimulation of the peripheral vagus nerve 6 because vagotomy abolishes the antiseizure effects of the drug. It is tempting to speculate that the ketogenic diet and certain antiepileptic drugs may owe part of their action to the PPAR–vagus-nerve–brain route. Given that the mechanism of many of the antiepileptic drugs developed throughout the past century remains either unknown or contested, it is imperative that procedures such as vagotomy become part of screening methods (eg, the pentylenetetrazol test) to determine the contributions of the peripheral and CNS to the actions of antiepileptic treatments. Tim Cullingford National Heart and Lung Institute, Imperial College London, UK. Email [email protected] more research is needed, especially in making telemedicine consumer- friendly and acceptable to staff. Stephen W Brown Peninsula Medical School Developmental Disabilities Research and Education Group, Unit 10 Bodmin Business Centre, Harleigh Road, Bodmin, Cornwall PL31 1AH, UK. Email [email protected] Conflict of interest SWB currently has a grant from the NHS Modernisation Agency ‘Action On Neurology’ Conflict of interest I have no conflicts of interest. References 1 Kossoff EH. More fat and fewer seizures: dietary therapies for epilepsy. Lancet Neurol 2004; 3: 415–20. 2 Theodore WH, Fisher RS. Brain stimulation for epilepsy. Lancet Neurol 2004; 3: 111–18. 3 Fu J, Gaetani S, Oveisi F, et al. Oleylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-alpha. Nature 2003; 425: 90–93. 4 Cullingford TE. Eagles DA, Sato H. The ketogenic diet upregulates expression of the gene encoding the key ketogenic enzyme mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase in rat brain. Epilepsy Res 2002; 49: 99–107. 5 Cullingford TE, The ketogenic diet; fatty acids, fatty acid-activated receptors and neurological disorders. Prostaglandins Leukot Essent Fatty Acids 2004; 70: 253–64. 6 Krahl SE, Senanayake SS, Handforth A. Seizure suppression by systemic epinephrine is mediated by the vagus nerve. Epilepsy Res 2000; 38: 171–75. Author’s reply This is certainly an interesting theory; there is much about the mechanisms of action of the ketogenic diet—and antiepileptic drugs for that matter— that remains unknown. However, there does not seem to be any effect of antiepileptic therapy, other than vagus- nerve stimulation, directly on the vagus nerve, and I suspect the ketogenic diet is unlikely to affect the CNS via this mechanism. Most of the children on the diet only have modest appetite suppression. In addition, ketosis, rather than calorie restriction, seems to be the predominant mechanism by which efficacy occurs. However, a clinical trial of oleoylethanolamide and other fatty acids to suppress seizures would certainly be of interest. Eric Kossoff The Johns Hopkins Medical Institution, Baltimore, Maryland, USA. Email [email protected] programme to develop telemedicine for epilepsy and dementia services in Cornwall. References 1 Grigoriev AI, Orlov OI. Telemedicine and spaceflight. Aviat Space Environ Med 2002; 73: 688–93. 2 Chua R, Craig J, Wootton R, Patterson V. Randomised controlled trial of telemedicine for new neurological outpatient referrals. J Neurol Neurosurg Psychiatry 2001; 71: 63–66. 3 Chua R, Craig J, Esmonde T, Wootton R, Patterson V. Telemedicine for new neurological outpatients: putting a randomized controlled trial in the context of everyday practice. J Telemed Telecare 2002; 8: 270–73. 4 Craig J, Chua R, Russell C, Wootton R, Chant D, Patterson V. A cohort study of early neurological consultation by telemedicine on the care of neurological inpatients. J Neurol Neurosurg Psychiatry 2004; 75: 1031–35. 5 Chua R, Craig J, Wootton R, Patterson V. Cost implications of outpatient teleneurology. J Telemed Telecare 2001; 7 (suppl 1): 62–64. 6 Mielonen ML, Ohinmaa A, Moring J, Isohanni M. Psychiatric inpatient care planning via telemedicine. J Telemed Telecare 2000; 6: 152–57. 7 Harrison R, Clayton W, Wallace P. Virtual outreach: a telemedicine pilot study using a cluster- randomized controlled design. J Telemed Telecare 1999; 5: 126–30. 8 Currell R, Urquhart C, Wainwright P, Lewis R. Telemedicine versus face to face patient care: effects on professional practice and health care outcomes (Cochrane Review). In: The Cochrane Library, Issue 2, 2004. Chichester, UK: John Wiley & Sons, Ltd. 9 Bergeron B. Telemedicine. MedGenMed 2003; 5: 43. 10 NHS to be first major public sector user of broadband. NHS National Programme for Information Technology. Press release http://www.dh.gov.uk/assetRoot/04/07/40/64/04074 064.pdf (accessed July 24, 2004).

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For personal use. Only reproduce with permission from Elsevier Ltd.518

Reflection & Reaction

Neurology Vol 3 September 2004 http://neurology.thelancet.com

The vagus nerve—a common route for epilepsy therapies?One mechanism not covered in therecent review by Eric Kossoff 1 is thatthe ketogenic diet (and othertreatments for epilepsy) may actindirectly on the brain via thesubabdominal left cervical-brain-stem–vagus-nerve route. Informationabout physiological factors (eg,appetite) travels along this nervebetween the brain and visceral organs,such as the liver and intestines. Externalelectrical stimulation of the left cervicalvagus nerve is an established treatmentfor epilepsy;2 antiepileptic drugs ordietary therapies may therefore exerttheir effect via internal stimulation ofthis route.

Diets rich in fatty acids and thosethat mimic fasting, such as theketogenic diet and the Atkin’s diet, haveappetite-suppressing effects. Recentstudies have shown that the fatty-acid-like molecule oleoylethanolamidesuppresses appetite through amechanism that is dependent on anintact vagus nerve.3 This effect ofoleoylethanolamide is also dependenton the presence of functionalperoxisome proliferator activatedreceptor alpha (PPAR�), probablylocated in the liver or the intestine incells adjacent to vagus-nerve afferents.3

PPAR� has been implicated in themetabolic effects of ketogenic diet orfasting on processes in the liver and thebrain,4 and, indeed, oleoylethanolamideis a ligand for PPAR�. Thus, it isproposed that the appetite suppressingeffects of oleoylethanolamide aremediated via activation of hepatic andintestinal PPAR�; these effects causechanges in cell state that stimulate the

neighbouring vagus-nerve afferents.Interpretation of such vagus-nervesignals in the hypothalamus results inappetite suppression via behaviouralmodifications.

In addition to oleoylethanolamide,PPAR� has an unusually broad range ofligands, including many fatty acids5

abundant in the ketogenic diet.Moreover, fatty-acid-like drugs, such asvalproic acid and several valproic-acidanalogues, activate PPAR�.6 There isalso a relation between potency ofPPAR� activation and antiseizureefficacy.5 This finding is particularlyintriguing because other antiepilepticdrugs may already be exploiting theinternal route of vagus-nervestimulation. Despite poor access to thebrain, the hormone epinephrine mayexert an antiseizure effect viastimulation of the peripheral vagusnerve6 because vagotomy abolishes theantiseizure effects of the drug.

It is tempting to speculate that theketogenic diet and certain antiepilepticdrugs may owe part of their action tothe PPAR�–vagus-nerve–brain route.Given that the mechanism of many ofthe antiepileptic drugs developedthroughout the past century remainseither unknown or contested, it isimperative that procedures such asvagotomy become part of screeningmethods (eg, the pentylenetetrazol test)to determine the contributions of theperipheral and CNS to the actions ofantiepileptic treatments.Tim Cullingford

National Heart and Lung Institute, ImperialCollege London, UK. Email [email protected]

more research is needed, especially in making telemedicine consumer-friendly and acceptable to staff. Stephen W Brown

Peninsula Medical School DevelopmentalDisabilities Research and EducationGroup, Unit 10 Bodmin Business Centre,Harleigh Road, Bodmin, Cornwall PL31 1AH, UK. Email [email protected]

Conflict of interestSWB currently has a grant from the NHSModernisation Agency ‘Action On Neurology’

Conflict of interestI have no conflicts of interest.

References1 Kossoff EH. More fat and fewer seizures: dietary

therapies for epilepsy. Lancet Neurol 2004;3: 415–20.

2 Theodore WH, Fisher RS. Brain stimulation forepilepsy. Lancet Neurol 2004; 3: 111–18.

3 Fu J, Gaetani S, Oveisi F, et al. Oleylethanolamideregulates feeding and body weight through activationof the nuclear receptor PPAR-alpha. Nature 2003;425: 90–93.

4 Cullingford TE. Eagles DA, Sato H. The ketogenicdiet upregulates expression of the gene encoding thekey ketogenic enzyme mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase in ratbrain. Epilepsy Res 2002; 49: 99–107.

5 Cullingford TE, The ketogenic diet; fatty acids, fattyacid-activated receptors and neurological disorders.Prostaglandins Leukot Essent Fatty Acids 2004;70: 253–64.

6 Krahl SE, Senanayake SS, Handforth A. Seizure suppression by systemic epinephrine ismediated by the vagus nerve. Epilepsy Res 2000;38: 171–75.

Author’s replyThis is certainly an interesting theory;there is much about the mechanisms of action of the ketogenic diet—andantiepileptic drugs for that matter—that remains unknown. However, theredoes not seem to be any effect ofantiepileptic therapy, other than vagus-nerve stimulation, directly on the vagusnerve, and I suspect the ketogenic diet is unlikely to affect the CNS viathis mechanism. Most of the childrenon the diet only have modest appetitesuppression. In addition, ketosis,rather than calorie restriction, seemsto be the predominant mechanism by which efficacy occurs. However, aclinical trial of oleoylethanolamideand other fatty acids to suppressseizures would certainly be of interest.Eric Kossoff

The Johns Hopkins Medical Institution,Baltimore, Maryland, USA. Email [email protected]

programme to develop telemedicine forepilepsy and dementia services in Cornwall.

References1 Grigoriev AI, Orlov OI. Telemedicine and

spaceflight. Aviat Space Environ Med 2002; 73:688–93.

2 Chua R, Craig J, Wootton R, Patterson V.Randomised controlled trial of telemedicine for newneurological outpatient referrals. J Neurol NeurosurgPsychiatry 2001; 71: 63–66.

3 Chua R, Craig J, Esmonde T, Wootton R, PattersonV. Telemedicine for new neurological outpatients:putting a randomized controlled trial in thecontext of everyday practice. J Telemed Telecare2002; 8: 270–73.

4 Craig J, Chua R, Russell C, Wootton R, Chant D,Patterson V. A cohort study of early neurologicalconsultation by telemedicine on the care ofneurological inpatients. J Neurol NeurosurgPsychiatry 2004; 75: 1031–35.

5 Chua R, Craig J, Wootton R, Patterson V. Cost implications of outpatient teleneurology. J Telemed Telecare 2001; 7 (suppl 1): 62–64.

6 Mielonen ML, Ohinmaa A, Moring J, Isohanni M.Psychiatric inpatient care planning via telemedicine.J Telemed Telecare 2000; 6: 152–57.

7 Harrison R, Clayton W, Wallace P. Virtual outreach:a telemedicine pilot study using a cluster-randomized controlled design. J Telemed Telecare1999; 5: 126–30.

8 Currell R, Urquhart C, Wainwright P, Lewis R.Telemedicine versus face to face patient care: effects on professional practice and health careoutcomes (Cochrane Review). In: The Cochrane Library, Issue 2, 2004. Chichester,UK: John Wiley & Sons, Ltd.

9 Bergeron B. Telemedicine. MedGenMed 2003; 5: 43.10 NHS to be first major public sector user of

broadband. NHS National Programme forInformation Technology. Press releasehttp://www.dh.gov.uk/assetRoot/04/07/40/64/04074064.pdf (accessed July 24, 2004).