Effects of bumetanide on neurobehavioral function in children and adolescents with autism spectrum disorders

Translational Psychiatry

Volumn 7, Issue 3, 2017, Pages

  Lemonnier, E ^a   Villeneuve, N ^b   Sonie, S ^c   Serret, S ^d   Rosier, A ^e   Roue, M ^f   Brosset, P ^a   Viellard, M ^b   Ernoux, D B ^c   Rondeau, S ^e   Thummler, S ^d   Ravel, D ^g   Ben Ari, Y ^g,h  

^a LIMOGES UNIVERSITY HOSPITAL   (France)

^b HÔPITAL SAINTE MARGUERITE   (France)

^c Hospital Centre le Vinatier   (France)

^d UNIVERSITY HOSPITAL OF NICE   (France)

^e CHS du Rouvray   (France)

^f BREST UNIVERSITY HOSPITAL   (France)

^g ASSISTANCE PUBLIQUE HÔPITAUX DE MARSEILLE   (France)

^h Turing Center for Living Systems CENTURI Aix Marseille University   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BUMETANIDE; PLACEBO; LOOP DIURETIC AGENT;

ABDOMINAL PAIN; ADOLESCENT; ADOLESCENT DISEASE; ADULT; ANOREXIA; ARTICLE; ASTHENIA; AUTISM; BELLY PAIN; BRAIN FUNCTION; CHILD; CHILDHOOD AUTISM RATING SCALE; CHILDHOOD DISEASE; CLINICAL GLOBAL IMPRESSION SCALE; CONTROLLED STUDY; DEHYDRATION; DIARRHEA; DIURESIS; DOSE RESPONSE; DOUBLE BLIND PROCEDURE; DRUG EFFECT; DRUG EFFICACY; DRUG SAFETY; ENURESIS; FATIGUE; FEMALE; GENERAL HEALTH STATUS ASSESSMENT; GROUPS BY AGE; HUMAN; HYPERURICEMIA; HYPOKALEMIA; LIQUID FECES; LOSS OF APPETITE; MAJOR CLINICAL STUDY; MALE; MULTICENTER STUDY; OPTIMAL DRUG DOSE; OUTCOME ASSESSMENT; PAIN; PHASE 2 CLINICAL TRIAL; POLLAKISURIA; POLYDIPSIA; POLYURIA; PRESCHOOL CHILD; RANDOMIZED CONTROLLED TRIAL; SIDE EFFECT; SOCIAL RESPONSIVE SCALE; THIRST; URINALYSIS; VOMITING; WEIGHT REDUCTION; CHEMICALLY INDUCED; CLINICAL TRIAL; PATHOPHYSIOLOGY; PSYCHOLOGY; TREATMENT OUTCOME;

ADOLESCENT; ANOREXIA; ASTHENIA; AUTISM SPECTRUM DISORDER; BUMETANIDE; CHILD; CHILD, PRESCHOOL; DEHYDRATION; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HUMANS; HYPOKALEMIA; MALE; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; TREATMENT OUTCOME;

EID: 85028504730     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2017.10     Document Type: Article

References (56)

1. Ben-Ari Y. The GABA excitatory/inhibitory developmental sequence: a personal journey. Neuroscience 2014; 279C: 187-219.
2. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 2002; 3: 728-739.
3. Boulenguez P, Liabeuf S, Bos R, Bras H, Jean-Xavier C, Brocard C et al. Downregulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat Med 2010; 16: 302-307.
4. Cohen I. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 2002; 298: 1418-1421.
5. Nardou R, Yamamoto S, Chazal G, Bhar A, Ferrand N, Dulac O et al. Neuronal chloride accumulation and excitatory GABA underlie aggravation of neonatal epileptiform activities by phenobarbital. Brain 2011; 134(Pt 4): 987-1002.
6. Kaila K, Price TJ, Payne JA, Puskarjov M, Voipio J. Cation-chloride cotransporters in neuronal development, plasticity and disease. Nat Rev Neurosci 2014; 15: 637-654.
7. Payne JA, Rivera C, Voipio J, Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 2003; 26: 199-206.
8. Barmashenko G, Schmidt M, Hoffmann K-P. Differences between cation-chloride co-transporter functions in the visual cortex of pigmented and albino rats. Eur J Neurosci 2005; 21: 1189-1195.
9. Pallud J, Le Van Quyen M, Bielle F, Pellegrino C, Varlet P, Labussiere M et al. Cortical GABAergic excitation contributes to epileptic activities around human glioma. Sci Transl Med 2014; 6: 244ra89.
10. Freund TF, Buzsaki G. Interneurons of the hippocampus. Hippocampus 1996; 6: 347-470.
11. Buzsaki G, Draguhn A. Neuronal oscillations in cortical networks. Science 2004; 304: 1926-1929.
12. Holmes GL, Tian C, Hernan AE, Flynn S, Camp D, Barry J. Alterations in sociability and functional brain connectivity caused by early-life seizures are prevented by bumetanide. Neurobiol Dis 2015; 77: 204-219.
13. Hasbargen T, Ahmed MM, Miranpuri G, Li L, Kahle KT, Resnick D et al. Role of NKCC1 and KCC2 in the development of chronic neuropathic pain following spinal cord injury. Ann N Y Acad Sci 2010; 1198: 168-172.
14. Seubert CN, Zhu W, Pavlinec C, Gravenstein N, Martynyuk AE. Developmental effects of neonatal isoflurane and sevoflurane exposure in rats. Anesthesiology 2013; 119: 358-364.
15. Feit PW. Bumetanide-the way to its chemical structure. J Clin Pharmacol 1981; 21: 531-536.
16. Flamenbaum W, Friedman R. Pharmacology, therapeutic efficacy, and adverse effects of bumetanide, a new 'loop' diuretic. Pharmacotherapy 1982; 2: 213-222.
17. Schopler E, Reichler RJ, DeVellis RF, Daly K. Toward objective classification of childhood autism - childhood autism rating-scale (CARS). J Autism Dev Disord 1980; 10: 91-103.
18. Autism Genome Project Consortium, Szatmari P, Paterson AD, Zwaigenbaum L, Roberts W, Brian J et al. Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat Genet 2007; 39: 319-328.
19. Bourgeron T. A synaptic trek to autism. Curr Opin Neurobiol 2009; 19: 231-234.
20. Glasson EJ, Bower C, Petterson B, de Klerk N, Chaney G, Hallmayer JF. Perinatal factors and the development of autism: a population study. Arch Gen Psychiatry 2004; 61: 618-627.
21. Gardener H, Spiegelman D, Buka SL. Prenatal risk factors for autism: comprehensive meta-analysis. Br J Psychiatry 2009; 195: 7-14.
22. Mann JR, McDermott S, Bao H, Hardin J, Gregg A. Pre-eclampsia, birth weight, and autism spectrum disorders. J Autism Dev Disord 2009; 40: 548-554.
23. Marrus N, Underwood-Riordan H, Randall F, Zhang Y, Constantino JN. Lack of effect of risperidone on core autistic symptoms: data from a longitudinal study. J Child Adolesc Psychopharmacol 2014; 24: 513-518.
24. Fung LK, Mahajan R, Nozzolillo A, Bernal P, Krasner A, Jo B et al. Pharmacologic treatment of severe irritability and problem behaviors in autism: a systematic review and meta-analysis. Pediatrics 2016; 137(Suppl 2): S124-S135.
25. Masi G, Cosenza A, Millepiedi S, Muratori F, Pari C, Salvadori F. Aripiprazole monotherapy in children and young adolescents with pervasive developmental disorders a retrospective study. CNS Drugs 2009; 23: 511-521.
26. Bear MF, Huber KM, Warren ST. The mGluR theory of fragile X mental retardation. Trends Neurosci 2004; 27: 370-377.
27. Krueger DD, Bear MF. Toward fulfilling the promise of molecular medicine in fragile X syndrome. Annu Rev Med 2011; 62: 411-429.
28. Berry-Kravis E, Hessl D, Coffey S, Hervey C, Schneider A, Yuhas J et al. A pilot open label, single dose trial of fenobam in adults with fragile X syndrome. J Med Genet 2009; 46: 266-271.
29. Berry-Kravis E, Portes des V, Hagerman R, Jacquemont S, Charles P, Visootsak J et al. Mavoglurant in fragile X syndrome: results of two randomized, double-blind, placebo-controlled trials. Sci Transl Med 2016; 8: 321ra5.
30. Berry-Kravis EM, Hessl D, Rathmell B, Zarevics P, Cherubini M, Walton-Bowen K et al. Effects of STX209 (arbaclofen) on neurobehavioral function in children and adults with fragile X syndrome: a randomized, controlled, phase 2 trial. Sci Transl Med 2012; 4: 152ra127.
31. Andari E, Duhamel J-R, Zalla T, Herbrecht E, Leboyer M, Sirigu A. Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proc Natl Acad Sci USA 2010; 107: 4389-4394.
32. Yatawara CJ, Einfeld SL, Hickie IB, Davenport TA, Guastella AJ. The effect of oxytocin nasal spray on social interaction deficits observed in young children with autism: a randomized clinical crossover trial. Mol Psychiatry 2015; 21: 1225-1231.
33. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hübner CA, Represa A et al. Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 2006; 314: 1788-1792.
34. Tyzio R, Nardou R, Ferrari DC, Tsintsadze T, Shahrokhi A, Eftekhari S et al. Oxytocinmediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring. Science 2014; 343: 675-679.
35. He Q, Nomura T, Xu J, Contractor A. The developmental switch in GABA polarity is delayed in fragile X mice. J Neurosci 2014; 34: 446-450.
36. Eftekhari S, Shahrokhi A, Tsintsadze V, Nardou R, Brouchoud C, Conesa M et al. Response to comment on 'Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring.'. Science 2014; 346: 176-176.
37. Lemonnier E, Degrez C, Phelep M, Tyzio R, Josse F, Grandgeorge M et al. A randomised controlled trial of bumetanide in the treatment of autism in children. Transl Psychiatry 2012; 2: e202.
38. Lemonnier E, Ben-Ari Y. The diuretic bumetanide decreases autistic behaviour in five infants treated during 3 months with no side effects. Acta Paediatr 2010; 99: 1885-1888.
39. Hadjikhani N, Zürcher NR, Rogier O, Ruest T, Hippolyte L, Ben-Ari Y et al. Improving emotional face perception in autism with diuretic bumetanide: a proof-of-concept behavioral and functional brain imaging pilot study. Autism 2015; 19: 149-157.
40. Bruining H, Passtoors L, Goriounova N, Jansen F, Hakvoort B, de Jonge M et al. Paradoxical benzodiazepine response: a rationale for bumetanide in neurodevelopmental disorders? Pediatrics 2015; 136: e539-e543.
41. Lemonnier E, Robin G, Degrez C, Tyzio R, Grandgeorge M, Ben-Ari Y. Treating Fragile X syndrome with the diuretic bumetanide: a case report. Acta Paediatr 2013; 102: e288-e290.
42. Du L, Shan L, Wang B, Li H, Xu Z, Staal WG et al. A pilot study on the combination of applied behavior analysis and bumetanide treatment for children with autism. J Child Adolesc Psychopharmacol 2015; 25: 585-588.
43. Ward A, Heel RC. Bumetanide. A review of its pharmacodynamic and pharmacokinetic properties and therapeutic use. Drugs 1984; 28: 426-464.
44. Lopez-Samblas AM, Adams JA, Goldberg RN, Modi MW. The pharmacokinetics of bumetanide in the newborn infant. Biol Neonate 1997; 72: 265-272.
45. Marshall JD, Wells TG, Letzig L, Kearns GL. Pharmacokinetics and pharmacodynamics of bumetanide in critically ill pediatric patients. J Clin Pharmacol 1998; 38: 994-1002.
46. Holazo AA, Colburn WA, Gustafson JH, Young RL, Parsonnet M. Pharmacokinetics of bumetanide following intravenous, intramuscular, and oral administrations to normal subjects. J Pharm Sci 1984; 73: 1108-1113.
47. Ramsay LE, McInnes GT, Hettiarachchi J, Shelton J, Scott P. Bumetanide and frusemide: a comparison of dose-response curves in healthy men. Br J Clin Pharmacol 1978; 5: 243-247.
48. Tuzel IH. Comparison of adverse reactions to bumetanide and furosemide. J Clin Pharmacol 1981; 21: 615-619.
49. Ares GR, Caceres PS, Ortiz PA. Molecular regulation of NKCC2 in the thick ascending limb. Am J Physiol Renal Physiol 2011; 301: F1143-F1159.
50. Dixon DW, Barwolf-Gohlke C, Gunnar RM. Comparative efficacy and safety of bumetanide and furosemide in long-term treatment of edema due to congestive heart failure. J Clin Pharmacol 1981; 21: 680-687.
51. Wells TG, Fasules JW, Taylor BJ, Kearns GL. Pharmacokinetics and pharmacodynamics of bumetanide in neonates treated with extracorporeal membrane oxygenation. J Pediatr 1992; 121: 974-980.
52. Ward OC, Lam LK. Bumetanide in heart failure in infancy. Arch Dis Child 1977; 52: 877-882.
53. Courchesne E, Mouton PR, Calhoun ME, Semendeferi K, hrens-Barbeau C, Hallet MJ et al. Neuron Number and size in prefrontal cortex of children with autism. JAMA 2011; 306: 2001-2010.
54. Thompson BL, Levitt P, Stanwood GD. Prenatal exposure to drugs: effects on brain development and implications for policy and education. Nat Rev Neurosci 2009; 10: 303-312.
55. Ben-Ari Y. Neuro-archaeology: pre-symptomatic architecture and signature of neurological disorders. Trends Neurosci 2008; 31: 626-636.
56. Orefice LL, Zimmerman AL, Chirila AM, Sleboda SJ, Head JP, Ginty DD. Peripheral mechanosensory neuron dysfunction underlies tactile and behavioral deficits in mouse models of ASDs. Cell 2016; 166: 299-313.