110
Views
7
CrossRef citations to date
0
Altmetric
Reviews

An update on congenital hyperinsulinism: advances in diagnosis and management

, , , , , , , , , , & show all

Bibliography

  • Dunne MJ, Cosgrove KE, Shepherd RM, et al. Hyperinsulinism in infancy from basic science to clinical disease. Physiol Rev 2004;84:239-75
  • Hussain K, Hindmarsh P, Aynsley-Green A. Neonates with symptomatic hyperinsulinemic hypoglycemia generate inappropriately low serum cortisol counterregulatory hormonal responses. J Clin Endocrinol Metab 2003;88(9):4342-7
  • Hussain K, Bryan J, Christesen HT, et al. Serum glucagon counterregulatory hormonal response to hypoglycemia is blunted in congenital hyperinsulinism. Diabetes 2005;54(10):2946-51
  • Gataullina S, Dellatolas G, Perdry H, et al. Comorbidity and metabolic context are crucial factors determining neurological sequelae of hypoglycaemia. Dev Med Child Neurol 2012;54(11):1012-17
  • Menni F, de Lonlay P, Sevin C, et al. Neurologic outcomes of 90 neonates and infants with persistent hyperinsulinemic hypoglycemia. Pediatrics 2001;107(3):476-9
  • Arnoux JB, Verkarre V, Saint-Martin C, et al. Congenital hyperinsulinism: current trends in diagnosis and therapy. Orphanet J Rare Dis 2011;6:63
  • de Lonlay P, Fournet JC, Touati G, et al. Heterogeneity of persistent hyperinsulinemic hypoglycemia of infancy. A series of 175 cases. Eur J Pediatr 2002;161:37-48
  • Banerjee I, Avatapalle B, Petkar A, et al. The association of cardiac ventricular hypertrophy with congenital hyperinsulinism. Eur J Endocrinol 2012;167(5):619-24
  • de Lonlay P, Cormier-Daire V, Amiel J, et al. Facial appearance in persistent hyperinsulinemic hypoglycemia. Am J Med Genet 2002;111(2):130-3
  • Al-Otaibi H, Senniappan S, Alam S, Hussain K. Biochemical studies in patients with hyperinsulinaemic hypoglycaemia. Eur J Pediatr 2013;172(11):1435-40
  • De León DD, Stanley CA. Determination of insulin for the diagnosis of hyperinsulinemic hypoglycemia. Best Pract Res Clin Endocrinol Metab 2013;27(6):763-9
  • Pørksen N, Nyholm B, Veldhuis JD, et al. In humans at least 75% of insulin secretion arises from punctuated insulin secretory bursts. Am J Physiol 1997;273:E908-14
  • Morishima T, Pye S, Bradshaw C, Radziuk J. Posthepatic rate of appearance of insulin: measurement and validation in the nonsteady state. Am J Physiol 1992;263:E772-9
  • Bonnefont JP, Specola NB, Vassault A, et al. The fasting test in paediatrics: application to the diagnosis of pathological hypo- and hyperketotic states. Eur J Pediatr 1990;150(2):80-5
  • Aynsley-Green A, Polak JM, Bloom SR, et al. Nesidioblastosis of the pancreas: definition of the syndrome and the management of the severe neonatal hyperinsulinaemic hypoglycaemia. Arch Dis Child 1981;56(7):496-508
  • Cryer PE, Axelrod L, Grossman AB, et al. Endocrine Society. Evaluation and management of adult hypoglycemic disorders: an Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab 2009;94(3):709-28
  • Peranteau WH, Palladino AA, Bhatti TR, et al. The surgical management of insulinomas in children. J Pediatr Surg 2013;48(12):2517-24
  • Placzkowski KE, Vella A, Tompson GB, et al. Secular trends in the presentation and management of functioning insulinoma at the Mayo Clinic 1987-2007. J Clin Endocrinol Metab 2009;94(4):1069-73
  • Kapoor RR, James C, Hussain K. Hyperinsulinism in developmental syndromes. Endocr Dev 2009;14:95-113
  • Kapoor RR, Flanagan SE, Arya VB, et al. Clinical and molecular characterisation of 300 patients with congenital hyperinsulinism. Eur J Endocrinol 2013;168(4):557-64
  • Lord K, Dzata E, Snider KE, et al. Clinical presentation and management of children with diffuse and focal hyperinsulinism: a review of 223 cases. J Clin Endocrinol Metab 2013;98(11):E1786-9
  • Kumaran A, Kapoor RR, Flanagan SE, et al. Congenital hyperinsulinism due to a compound heterozygous ABCC8 mutation with spontaneous resolution at eight weeks. Horm Res Paediatr 2010;73(4):287-92
  • Abdulhadi-Atwan M, Bushman J, Tornovsky-Babaey S, et al. Novel de novo mutation in sulfonylurea receptor 1 presenting as hyperinsulinism in infancy followed by overt diabetes in early adolescence. Diabetes 2008;57(7):1935-40
  • Bahi-Buisson N, Roze E, Dionisi C, et al. Neurological aspects of hyperinsulinism-hyperammonaemia syndrome. Dev Med Child Neurol 2008;50(12):945-9
  • Stanescu DE, Hughes N, Kaplan B, et al. Novel presentations of congenital hyperinsulinism due to mutations in the MODY genes: HNF1A and HNF4A. J Clin Endocrinol Metab 2012;97(10):E2026-30
  • Ban N, Yamada Y, Someya Y, et al. Hepatocyte nuclear factor-1alpha recruits the transcriptional co-activator p300 on the GLUT2 gene promoter. Diabetes 2002;51(5):1409-18
  • Stoffel M, Duncan SA. The maturity-onset diabetes of the young (MODY1) transcription factor HNF4alpha regulates expression of genes required for glucose transport and metabolism. Proc Natl Acad Sci USA 1997;94:13209-14
  • Hoffman TL, Blanco E, Lane A, et al. Glucose metabolism and insulin secretion in a patient with ABCC8 mutation and Fanconi-Bickel syndrome caused by maternal isodisomy of chromosome 3. Clin Genet 2007;71(6):551-7
  • Albaqumi M, Alhabib FA, Shamseldin HE, et al. A syndrome of congenital hyperinsulinism and rhabdomyolysis is caused by KCNJ11 mutation. J Med Genet 2014, doi:10.1136/jmedgenet-2013-102085
  • Padidela R, Kapoor RR, Moyo Y, et al. Focal congenital hyperinsulinism in a patient with septo-optic dysplasia. Nat Rev Endocrinol 2010;6(11):646-50
  • Calton EA, Temple IK, Mackay DJ, et al. Hepatoblastoma in a child with a paternally-inherited ABCC8 mutation and mosaic paternal uniparental disomy 11p causing focal congenital hyperinsulinism. Eur J Med Genet 2013;56(2):114-17
  • Pinney SE, Ganapathy K, Bradfield J, et al. Dominant form of congenital hyperinsulinism maps to HK1 region on 10q. Horm Res Paediatr 2013;80(1):18-27
  • Bellanné-Chantelot C, Saint-Martin C, Ribeiro MJ, et al. ABCC8 and KCNJ11 molecular spectrum of 109 patients with diazoxide-unresponsive congenital hyperinsulinism. J Med Genet 2010;47(11):752-9
  • Snider KE, Becker S, Boyajian L, et al. Genotype and phenotype correlations in 417 children with congenital hyperinsulinism. J Clin Endocrinol Metab 2013;98(2):E355-63
  • Arnoux JB, Verkarre V, Rossignol S, et al. Molecular mechanisms and clinical pathophysiologies of Focal ATP-sensitive potassium channel hyperinsulinism and beckwith-wiedemann syndrome. Basel: monogenic hyperinsulinemic hypoglycemia disorders. Front Diabetes 2012;21:43-56
  • Ismail D, Smith VV, de Lonlay P, et al. Familial focal congenital hyperinsulinism. J Clin Endocrinol Metab 2011;96(1):24-8
  • Valayannopoulos V, Romano S, Mention K, et al. What’s new in metabolic and genetic hypoglycaemias: diagnosis and management. Eur J Pediatr 2008;167(3):257-65
  • Flanagan SE, Kapoor RR, Banerjee I, et al. Dominantly acting ABCC8 mutations in patients with medically unresponsive hyperinsulinaemic hypoglycaemia. Clin Genet 2011;79(6):582-7
  • Shemer R, Avnon Ziv C, Laiba E, et al. Relative expression of a dominant mutated ABCC8 allele determines the clinical manifestation of congenital hyperinsulinism. Diabetes 2012;61(1):258-63
  • Kapoor RR, Flanagan SE, Ellard S, Hussain K. Congenital hyperinsulinism: marked clinical heterogeneity in siblings with identical mutations in the ABCC8 gene. Clin Endocrinol (Oxf) 2012;76(2):312-13
  • Rahier J, Guiot Y, Sempoux C. Morphologic analysis of focal and diffuse forms of congenital hyperinsulinism. Semin Pediatr Surg 2011;20(1):3-12
  • de Lonlay P, Fournet JC, Rahier J, et al. Somatic deletion of the imprinted 11p15 region in sporadicpersistent hyperinsulinemic hypoglycemia of infancy is specific of focal adenomatous hyperplasia and endorses partial pancreatectomy. J Clin Invest 1997;100(4):802-7
  • Hussain K, Seppänen M, Näntö-Salonen K, et al. The diagnosis of ectopic focal hyperinsulinism of infancy with [18F]-dopa positron emission tomography. J Clin Endocrinol Metab 2006;91(8):2839-42
  • Peranteau WH, Bathaii SM, Pawel B, et al. Multiple ectopic lesions of focal islet adenomatosis identified by positron emission tomography scan in an infant with congenital hyperinsulinism. J Pediatr Surg 2007;42(1):188-92
  • Laje P, Palladino AA, Bhatti TR, et al. Pancreatic surgery in infants with Beckwith-Wiedemann syndrome and hyperinsulinism. J Pediatr Surg 2013;48(12):2511-16
  • Suchi M, MacMullen CM, Thornton PS, et al. Molecular and immunohistochemical analyses of the focal form of congenital hyperinsulinism. Mod Pathol 2006;19(1):122-9
  • Giurgea I, Sanlaville D, Fournet JC, et al. Congenital hyperinsulinism and mosaic abnormalities of the ploidy. J Med Genet 2006;43(3):248-54
  • Ernst LE, Suchi M, Stanley CA, et al. Localized islet cell nuclear enlargement in congenital hyperinsulinism: a distinct clinicopathologic entity. Soc Pediatr Pathol Spring Meeting 2007. Available from: http://www.spponline.org/abstracts2007.pdf
  • Sempoux C, Capito C, Bellanné-Chantelot C, et al. Morphological mosaicism of the pancreatic islets: a novel anatomopathological form of persistent hyperinsulinemic hypoglycemia of infancy. J Clin Endocrinol Metab 2011;96(12):3785-93
  • Henquin JC, Sempoux C, Marchandise J, et al. Congenital hyperinsulinism caused by hexokinase I expression or glucokinase-activating mutation in a subset of β-cells. Diabetes 2013;62(5):1689-96
  • Hussain K, Blankenstein O, De Lonlay P, Christesen HT. Hyperinsulinaemic hypoglycaemia: biochemical basis and the importance of maintaining normoglycaemia during management. Arch Dis Child 2007;92:568-70
  • Yildizdas D, Erdem S, Küçükosmanoglu O, et al. Pulmonary hypertension, heart failure and neutropenia due to diazoxide therapy. Adv Ther 2008;25(5):515-19
  • Yoshida K, Kawai M, Marumo C, et al. High prevalence of severe circulary complications with diazoxide in premature infants. Neonatalogy 2014;105(3):166-71
  • Laje P, Halaby L, Adzick NS, Stanley CA. Necrotizing enterocolitis in neonates receiving octreotide for the management of congenital hyperinsulinism. Pediatr Diabetes 2010;11(2):142-7
  • Avatapalle B, Padidela R, Randell T, Banerjee I. Drug-induced hepatitis following use of octreotide for long-term treatment of congenital hyperinsulinism. BMJ Case Rep 2012, doi:10.1136/bcr-2012-006271
  • Celik N, Cinaz P, Emeksiz HC, et al. Octreotide-induced long QT syndrome in a child with congenital hyperinsulinemia and a novel missense mutation (p.Met115Val) in the ABCC8 gene. Horm Res Paediatr 2013;80(4):299-303
  • Banerjee I, Skae M, Flanagan SE, et al. The contribution of rapid KATP channel gene mutation analysis to the clinical management of children with congenital hyperinsulinism. Eur J Endocrinol 2011;164(5):733-40
  • Ribeiro MJ, De Lonlay P, Delzescaux T, et al. Characterization of hyperinsulinism in infancy assessed with PET and 18F-fluoro-L-DOPA. J Nucl Med 2005;46:560-6
  • Treglia G, Mirk P, Rufini V. Diagnostic performance of fluorine-18-dihydroxyphenylalanine positron emission tomography in diagnosing and localizing the focal form of congenital hyperinsulinism. Pediatr Radiol 2012;42(11):1372-9
  • Chigot V, de Lonlay P, Nassogne MC, et al. Pancreatic arterial calcium stimulation in the diagnosis and localsation od persistent hyperinsulinemic hypoglycaemia of infancy. Pediatr Radiol 2001;31(9):650-5
  • Mohnike K, Blankenstein O, Christesen HT, et al. Proposal for a standardized protocol for 18F-DOPA-PET (PET/CT) in congenital hyperinsulinism. Horm Res 2006;66(1):40-2
  • Otonkoski T, Nanto-Salonen K, Seppanen M, et al. Noninvasive diagnosis of focal hyperinsulinism of infancy with [18F]-DOPA positron emission tomography. Diabetes 2006;55(1):13-18
  • Hardy OT, Hernandez-Pampaloni M, Saffer JR, et al. Accuracy of [18F]fluorodopa positron emission tomography for diagnosing and localizing focal congenital hyperinsulinism. J Clin Endocrinol Metab 2007;92(12):4706-11
  • Bier DM, Leake RD, Haymond MW, et al. Measurement of "true" glucose production rates in infancy and childhood with 6,6-dideuteroglucose. Diabetes 1977;26(11):1016-23
  • Marks V, Teale JD. Drug-induced hypoglycemia. Endocrinol Metab Clin North Am 1999;28(3):555-77
  • Rabiee A, Magruber JT, Salas-Carrillo R, et al. Hyperinsulinemic hypoglycemia after Roux-en-Y gastric bypass: unraveling the role of gut hormonal and pancreatic endocrine dysfunction. J Surg Res 2011;167:199-205
  • Service GJ, Thompson GB, Service FJ, et al. Hyperinsulinemic hypoglycemia with nesidioblastosis after gastric-bypass surgery. N Engl J Med 2005;353:249-54
  • Roberts RE, Zhao M, Whitelaw BC, et al. GLP-1 and glucagon secretion from pancreatic neuroendocrine tumor causing diabetes and hyperinsulinemic hypoglycemia. J Clin Endocrinol Metab 2012;97(9):3039-45
  • Farina MI, Scarani R, Po’ C, et al. Congenital central hypoventilation syndrome and hypoglycaemia. Acta Paediatr 2012;101(2):e92-6
  • Marks V, Teale JD. Tumors producing hypoglycaemia. Endocrine Rel Cancer 1998;5:111-29
  • O’Rahilly S, Gray H, Humphreys PJ, et al. Brief report: impaired processing of prohormones associated with abnormalities of glucose homeostasis and adrenal function. N Eng J Med 1995;333:1386-90
  • Fukuda I, Hizuka N, Ishikawa Y, et al. Clinical features of insulin-like growth factor-II producing non-islet-cell tumor hypoglycemia. Growth Horm IGF Res 2006;16(4):211-16
  • Nauck MA, Reinecke M, Perren A, et al. Hypoglycemia due to paraneoplastic secretion of insulin- like growth factor-I in a patient with metastasizing large- cell carcinoma of the lung. J Clin Endocrinol Metab 2007;92:1600-5
  • Lupsa BS, Chong AY, Cochran EK, et al. Autoimmune forms of hypoglycemia. Medicine 2009;88(3):141-53
  • Kawashima Y, Nishimura R, Utsunomiya A, et al. Leprechaunism (Donohue syndrome): a case bearing novel compound heterozygous mutations in the insulin receptor gene. Endocr J 2013;60(1):107-12
  • Hussain K, Challis B, Rocha N, et al. An activating mutation of AKT2 and human hypoglycemia. Science 2011;334(6055):474
  • Hussain K, Cosgrove KE, Sheperd RM, et al. Hyperinsulinemic hypoglycaemia in Beckwith-Wiedemann syndrome due to defects in the function of pancreatic beta-cell adenosine triphosphate-sensitive potassium channels. J Clin Endocrinol Metab 2005;90(7):4376-82
  • Henneveld HT, van Lingen RA, Hamel BC, et al. Perlman syndrome: four additional cases and review. Am J Med Genet 1999;86(5):439-46
  • Matsuo T, Ihara K, Ochiai M, et al. Hyperinsulinemic hypoglycemia of infancy in Sotos syndrome. Am J Med Genet A 2013;161A(1):34-7
  • Bereket A, Turan S, Alper G, et al. Two patients with Kabuki syndrome presenting with endocrine problems. J Pediatr Endocrinol Metab 2001;14:215-20
  • de Lonlay P, Cuer M, Vuillaumier-Barrot S, et al. Hyperinsulinemic hypoglycemia as a presenting sign in phosphomannose isomerase deficiency: a new manifestation of carbohydrate-deficient glycoprotein syndrome treatable with mannose. J Pediatr 1999;135:379-83
  • Alexander S, Ramadan D, Alkhayyat H, et al. Costello syndrome and hyperinsulinemic hypoglycemia. Am J Med Genet A 2005;139(3):227-30
  • Hennewig U, Hadzik B, Vogel M, et al. Congenital central hypoventilation syndrome with hyperinsulinism in a preterm infant. J Hum Genet 2008;53(6):573-7
  • Bitner-Glindzicz M, Lindley KJ, Rutland P, et al. A recessive contiguous gene deletion causing infantile hyperinsulinism, enteropathy and deafness identifies the Usher type IC gene. Nat Genet 2000;26:56-60
  • Alkhayyat H, Christesen HB, Steer J, et al. Mosaic Turner syndrome and hyperinsulinaemic hypoglycaemia. J Pediatr Endocrinol Metab 2006;19(12):1451-7
  • de Lonlay-Debeney P, Poggi-Travert F, Fournet JC, et al. Clinical features of 52 neonates with hyperinsulinism. N Engl J Med 1999;340(15):1169-75
  • Suchi M, Thornton PS, Adzick NS, et al. Congenital hyperinsulinism: intraoperative biopsy interpretation can direct the extent of pancreatectomy. Am J Surg Pathol 2004;28(10):1326-35
  • Laje P, Stanley CA, Palladino AA, et al. Pancreatic head resection and Roux-en-Y pancreaticojejunostomy for the treatment of the focal form of congenital hyperinsulinism. J Pediatr Surg 2012;47(1):130-5
  • Khen-Dunlop N, Capito C, Valayannopoulos V, et al. Predictive value of postoperative glycosuria after partial elective pancreatectomy in focal congenital hyperinsulinism. Diabetes Care 2008;31(10):e71
  • Modan-Moses D, Koren I, Mazor-Aronovitch K, et al. Treatment of congenital hyperinsulinism with lanreotide acetate (Somatuline Autogel). J Clin Endocrinol Metab 2011;96(8):2312-17
  • Le Quan Sang KH, Arnoux JB, Mamoune A, et al. Successful treatment of congenital hyperinsulinism with long-acting release octreotide. Eur J Endocrinol 2012;166(2):333-9
  • Astruc B, Marbach P, Bouterfa H, et al. Long-acting octreotide and prolonged-release lanreotide formulations have different pharmacokinetic profiles. J Clin Pharmacol 2005;45(7):836-44
  • Kühnen P, Marquard J, Ernert A, et al. Long-term lanreotide treatment in six patients with congenital hyperinsulinism. Horm Res Paediatr 2012;78(2):106-12
  • Burman P, Besjakov J, Svensjö T. Large fat and skin necroses after deep subcutaneous injections of a slow-release somatostatin analogue in a woman with acromegaly. Growth Horm IGF Res 2010;20(6):438-40
  • Filan PM, Inder TE, Cameron FJ, et al. Neonatal hypoglycemia and occipital cerebral injury. J Pediatr 2006;148:552-5
  • Gataullina S, De Lonlay P, Dellatolas G, et al. Topography of brain damage in metabolic hypoglycaemia is determined by age at which hypoglycaemia occurred. Dev Med Child Neurol 2013;55(2):162-6
  • Tornovsky-Babeay S, Dadon D, Ziv O, et al. Type 2 diabetes and congenital hyperinsulinism cause DNA double-strand breaks and p53 activity in beta cells. Cell Metab 2013, doi:10.1016/j.cmet.2013.11.007
  • Beltrand J, Caquard M, Arnoux JB, et al. Glucose metabolism in 105 children and adolescents after pancreatectomy for congenital hyperinsulinism. Diabetes Care 2012;35(2):198-203
  • Maiorana A, Barbetti F, Boiani A, et al. Focal congenital hyperinsulinism managed by medical treatment: a diagnostic algorithm based on molecular genetic screening. Clin Endocrinol (Oxf) 2014, doi:10.1111/cen.12400
  • Schutz PW, Struys EA, Sinclair G, Stockler S. Protective effects of d-3-hydroxybutyrate and propionate during hypoglycemic coma: clinical and biochemical insights from infant rats. Mol Genet Metab 2011;103(2):179-84
  • Stevens A, Cosgrove KE, Padidela R, et al. Can network biology unravel the aetiology of congenital hyperinsulinism? Orphanet J Rare Dis 2013;8(1):21
  • Pinney SE, MacMullen C, Becker S, et al. Clinical characteristics and biochemical mechanisms of congenital hyperinsulinism associated with dominant KATP channel mutation. J Clin Invest 2008;118(8):2877-86
  • Masue M, Nishibori H, Fukuyama S, et al. Diagnostic accuracy of [¹8F]-fluoro-L-dihydroxyphenylalanine positron emission tomography scan for persistent congenital hyperinsulinism in Japan. Clin Endocrinol (Oxf) 2011;75(3):342-6
  • Dutta S, Venkataseshan S, Bal C, et al. Novel use of somatostatin receptor scintigraphy in localization of focal congenital hyperinsulinism: promising but fallible. J Pediatr Endocrinol Metab 2009;22(10):965-9
  • Yadav D, Dhingra B, Kumar S, et al. Persistent hyperinsulinemic hypoglycemia of infancy. J Pediatr Endocrinol Metab 2012;25(5-6):591-3
  • von Rohden L, Mohnike K, Mau H, et al. Visualization of the focus in congenital hyperinsulinism by intraoperative sonography. Semin Pediatr Surg 2011;20(1):28-31
  • Yorifuji T, Kawakita R, Hosokawa Y, et al. Efficacy and safety of long-term, continuous subcutaneous octreotide infusion for patients with different subtypes of KATP-channel hyperinsulinism. Clin Endocrinol (Oxf) 2013;78(6):891-7
  • Levy-Shraga Y, Pinhas-Hamiel O, Kraus-Houminer E, et al. Cognitive and developmental outcome of conservatively treated children with congenital hyperinsulinism. J Pediatr Endocrinol Metab 2013;26(3-4):301-8
  • Senniappan S, Alexandrescu S, Tatevian N, et al. Sirolimus therapy in infants with severe hyperinsulinemic hypoglycemia. N Engl J Med 2014;370(12):1131-7
  • Martin GM, Chen PC, Devaraneni P, Shyng SL. Pharmacological rescue of trafficking-impaired ATP-sensitive potassium channels. Front Physiol 2013;4:386
  • Powell PD, Bellanné-Chantelot C, Flanagan SE, et al. In vitro recovery of ATP-sensitive potassium channels in beta-cells from patients with congenital hyperinsulinism of infancy. Diabetes 2011;60(4):1223-8
  • Mohnike K, Blankenstein O, Pfuetzner A, et al. Long-term non-surgical therapy of severe persistent congenital hyperinsulinism with glucagon. Horm Res 2008;70(1):59-64
  • Calabria AC, Li C, Gallagher PR, et al. GLP-1 receptor antagonist exendin-(9-39) elevates fasting blood glucose levels in congenital hyperinsulinism owing to inactivating mutations in the ATP-sensitive K+ channel. Diabetes 2012;61:2585-91
  • Corbin J, Bhaskar V, Goldfine ID, et al. Inhibition of insulin receptor function by a human, allosteric monoclonal antibody: a potential new approach for the treatment of hyperinsulinemic hypoglycemia. MAbs 2014;6(1):262-72

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.