Neonatal hyperinsulinism: clinicopathologic correlation

Human Pathology

Volumn 38, Issue 3, 2007, Pages 387-399

  Delonlay, P ^a   Simon, A ^a   Galmiche Rolland, L ^a   Giurgea, I ^b   Verkarre, V ^a   Aigrain, Y ^a   Santiago Ribeiro, M J ^c   Polak, M ^a   Robert, J J ^a   Bellanne Chantelot, C ^d   Brunelle, F ^a   Nihoul Fekete, C ^a   Jaubert, F ^a  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

^b HENRI MONDOR HOSPITAL   (France)

^c DIF   (France)

^d HÔPITAL SAINT ANTOINE   (France)

Author keywords

cell; Hyperinsulinism; K channel

Indexed keywords

CONTRAST MEDIUM; DIHYDROXYPHENYLALANINE F 18; POTASSIUM CHANNEL; SULFONYLUREA RECEPTOR 1; UNCLASSIFIED DRUG;

ARTICLE; AUTOSOMAL RECESSIVE INHERITANCE; BECKWITH WIEDEMANN SYNDROME; CHROMOSOME 11; DIABETES MELLITUS; DISOMY; FATHER; FROZEN SECTION; GENETIC ASSOCIATION; HETEROZYGOSITY LOSS; HUMAN; HUMAN TISSUE; NEWBORN; PANCREAS INSUFFICIENCY; PANCREAS RESECTION; PATHOGENESIS; PERSISTENT HYPERINSULINEMIC HYPOGLYCEMIA OF INFANCY; POSITRON EMISSION TOMOGRAPHY; PREOPERATIVE EVALUATION; TREATMENT INDICATION; TREATMENT OUTCOME;

ATP-BINDING CASSETTE TRANSPORTERS; BIOPSY; FROZEN SECTIONS; HUMANS; INFANT; INFANT, NEWBORN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MUNCHAUSEN SYNDROME; NESIDIOBLASTOSIS; PANCREAS; PERSISTENT HYPERINSULINEMIA HYPOGLYCEMIA OF INFANCY; POTASSIUM CHANNELS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RECEPTORS, DRUG;

EID: 33846927989     PISSN: 00468177     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.humpath.2006.12.007     Document Type: Article

References (69)

1. Le Lay J., Matsuoka T.-A., Henderson E., and Stein R. Identification of a novel PDX-1 binding site in the human insulin gene enhancer. J Biol Chem 279 (2003) 22228-22235
2. Hernandez-Sanchez C., De La Rosa E.J., Mansilla A., and De Pablo F. Proinsulin in development: new roles for an ancient prohormone. Diabetologia 49 (2006) 1142-1150
3. Rahier J., Wallon J., and Henquin J.C. Cell populations in the endocrine pancreas of human neonates and infants. Diabetologia 20 (1981) 540-546
4. Heitz P.U., Kloppel G., Haecki W.H., Polak J., and Pearse A.G.E. Nesidioblastosis: the pathologic basis of persistent hyperinsulinemic hypoglycemia in infants. Diabetes 26 (1977) 632-642
5. Gould V.E., Memoli V.A., Dardi L.E., and Gould N.S. Nesidiodysplasia and nesidioblastosis of infancy: structural and functional correlations with the syndrome of hyperinsulinemic hypoglycemia. Ped Pathol 1 (1983) 7-31
6. Like A.A., and Orcil L. Embryogenesis of the human pancreatic islets: a light and electron microscopy study. Diabetes 21 Suppl. 2 (1972) 511-534
7. Ehrie M.G., and Swartz F.J. Diploid, tetraploid and octaploid beta cells in the islets of Langerhans of the normal human pancreas. Diabetes 23 (1974) 583-588
8. Rahier J., Falt K., Muntefering H., Becker K., Gepts W., and Falkmer S. The basic structural lesion of persistent neonatal hypoglycemia with hyperinsulinism: deficiency of pancreatic D cells or hyperactivity of B cells?. Diabetologia 26 (1984) 282-289
9. Ariel I., Kerem E., Schwartz-Arad D., et al. Nesidiodysplasia-a histologic entity. Hum Pathol 19 (1988) 1215-1218
10. Hultquist G.T., and Olding L.B. Endocrine pathology of infants of diabetic mothers: a quantitative morphological analysis including comparisons with infants of isoimmunized and non diabetic mothers. Acta Endocrinol 97 Suppl 241 (1981) 1-202
11. Gepts W., and De Mey J. Islet cell survival determined by morphology: an immunocytochemical study of the islets of Langerhans in juvenile diabetes mellitus. Diabetes 27 Suppl (1978) 251-261
12. Rahier J., Goebbels R.M., and Henquin J.C. Cellular composition of the human diabetic pancreas. Diabetologia 24 (1983) 366-371
13. Goossens A., Gepts W., Saudubray J.-M., et al. Diffuse and focal nesidioblastosis: a clinicopathological study of 24 patients with persistent neonatal hyperinsulinemic hypoglycemia. Am J Surg Pathol 13 (1989) 766-775
14. de Lonlay-Debeney P., Poggi-Travert F., Fournet J.C., et al. Clinical features of 52 neonates with hyperinsulinism. N Engl J Med 340 (1999) 1169-1175
15. Ferry Jr. R.J., Kelly A., Grimberg A., et al. Calcium-stimulated insulin secretion in diffuse and focal forms of congenital hyperinsulinism. J Pediatr 137 (2000) 239-246
16. Giurgea I., Laborde K., Touati G., et al. Acute insulin responses to calcium and tolbutamide do not differentiate focal from diffuse congenital hyperinsulinism. J Clin Endocrinol Metab 89 (2004) 925-929
17. Ribeiro M.J., De Lonlay P., Delzescaux T., et al. Characterization of hyperinsulinism in infancy assessed with PET and 18F-fluoro-L-DOPA. J Nucl Med 46 (2005) 560-566
18. Adzick N.S., Thornton P.S., Stanley C.A., Kaye R.D., and Ruchelli E. A multidisciplinary approach to the focal form of congenital hyperinsulinism leads to successful treatment by partial pancreatectomy. J Pediatr Surg 39 (2004) 270-275
19. Suchi M., Thornton P.S., Adzick N.S., et al. Congenital hyperinsulinism: intraoperative biopsy interpretation can direct the extent of pancreatectomy. Am J Surg Pathol 28 (2004) 1326-1335
20. Rahier J., Sempoux C., Fournet J.C., et al. Partial or near-total pancreatectomy for persistent neonatal hyperinsulinaemic hypoglycaemia: the pathologist's role. Histopathology 32 (1998) 15-19
21. Fekete C.N., de Lonlay P., Jaubert F., Rahier J., Brunelle F., and Saudubray J.M. The surgical management of congenital hyperinsulinemic hypoglycemia in infancy. J Pediatr Surg 39 (2004) 267-269
22. Sempoux C., Guiot Y., Dahan K., et al. The focal form of persistent hyperinsulinemic hypoglycemia of infancy: morphological and molecular studies show structural and functional differences with insulinoma. Diabetes 52 (2003) 784-794
23. Sempoux C., Guiot Y., Jaubert F., and Rahier J. Focal and diffuse forms of congenital hyperinsulinism: the keys for differential diagnosis. Endocr Pathol 15 (2004) 241-246
24. Suchi M., MacMullen C.M., Thornton P.S., et al. Molecular and immunohistochemical analyses of the focal form of congenital hyperinsulinism. Mod Pathol 19 (2006) 122-129
25. Sempoux C., Guiot Y., Lefevre A., et al. Neonatal hyperinsulinemic hypoglycemia: heterogeneity of the syndrome and keys for differential diagnosis. J Clin Endocrinol Metab 83 (1998) 1455-1461
26. Giurgea I., Sempoux C., Bellanne-Chantelot C., et al. The Knudson's two-hit model and timing of somatic mutation may account for the phenotypic diversity of focal congenital hyperinsulinism. J Clin Endocrinol Metab 91 (2006) 4118-4123
27. Giurgea I., Sanlaville D., Fournet J.C., et al. Congenital hyperinsulinism and mosaic abnormalities of the ploidy. J Med Genet 43 (2006) 248-254
28. Hussain K.C., Cosgrove K.E., Shepherd R.M., et al. Hyperinsulinemic hypoglycemia in Beckwith-Wiedemann syndrome due to defects in the function of pancreatic beta-cell adenosine triphosphate-sensitive potassium channels. J Clin Endocrinol Metab 90 (2005) 4376-4382
29. Giurgea I., Ulinski T., Touati G., et al. Factitious hyperinsulinism leading to pancreatectomy: severe forms of Munchausen syndrome by proxy. Pediatrics 116 (2005) 145-148
30. Service F.J., Natt N., Thompson G.B., et al. Noninsulinoma pancreatogenous hypoglycemia: a novel syndrome of hyperinsulinemic hypoglycemia in adults independant of mutations in Kir6.2 and SUR1 genes. J Clin Endocrinol Metab 84 (1999) 1582-1589
31. Service G.J., Thompson G.B., Service F.J., Andrews J.C., Collazo-Clavell M.L., and Lloyd R.V. Hyperinsulinemic hypoglycemia with nesidioblastosis after gastric-bypass surgery. N Engl J Med 353 (2005) 249-254
32. Witteles R.M., Straus F.H., Sugg S.L., Koka M.R., Costa E.A., and Kaplan E.L. Adult-onset nesidioblastosis causing hypoglycemia. Arch Surg 136 (2001) 656-663
33. Anlauf M., Wieben D., Perren A., et al. Persistent hyperinsulinemic hypoglycemia in 15 adults with diffuse nesidioblastosis: diagnostic criteria, incidence, and characterization of beta-cell changes. Am J Surg Pathol 29 (2005) 524-533
34. Goudswaard W.B., Houthoff H.J., Koudstaal J., and Zwiersta R.P. Nesidioblastosis and endocrine hyperplasia of the pancreas: a secondary phenomenon. Hum Pathol 17 (1986) 46-53
35. Suchi M., MacMullen C., Thornton P.S., Ganguly A., Stanley C.A., and Ruchelli E.D. Histopathology of congenital hyperinsulinism: retrospective study with genotype correlations. Pediatr Dev Pathol 6 (2003) 322-333
36. Giurgea I., Bellanne-Chantelot C., Ribeiro M., et al. Molecular mechanisms of neonatal hyperinsulinism. Horm Res 66 (2006) 289-296
37. Glaser B., Chiu K.C., Anker R., et al. Familial hyperinsulinism maps to chromosome 11p14-15.1, 30 cM centromeric to the insulin gene. Nat Genet 7 (1994) 185-188
38. Glaser B., Chiu K.C., Liu L., et al. Recombinant mapping of the familial hyperinsulinism gene to an 0.8 cM region on chromosome 11p15.1 and demonstration of a founder effect in Ashkenazi Jews. Hum Mol Genet 4 (1995) 879-886
39. Grimberg A., Ferry R.J., Kelly A., et al. Dysregulation of insulin secretion in children with congenital hyperinsulinism due to sulfonylurea receptor mutations. Diabetes 50 (2001) 322-328
40. Kane C., Shepherd R.M., Squires P.E., et al. Loss of functional KATP channels in pancreatic beta-cells causes persistent hyperinsulinemic hypoglycemia of infancy. Nat Med 2 (1996) 1344-1347
41. Glaser B., Ryan F., Donath M., et al. Hyperinsulinism caused by paternal-specific inheritance of a recessive mutation in the sulfonylurea-receptor gene. Diabetes 48 (1999) 1652-1657
42. Nestorowicz A., Wilson B.A., Schoor K.P., et al. Mutations in the sulonylurea receptor gene are associated with familial hyperinsulinism in Ashkenazi Jews. Hum Mol Genet 5 (1996) 1813-1822
43. Otonkoski T., Ammälä C., Huopio H., et al. A point mutation inactivating the sulfonylurea receptor causes the severe form of persistent hyperinsulinemic hypoglycemia of infancy in Finland. Diabetes 48 (1999) 408-415
44. Henwood M.J., Kelly A., Macmullen C., et al. Genotype-phenotype correlations in children with congenital hyperinsulinism due to recessive mutations of the adenosine triphosphate-sensitive potassium channel genes. J Clin Endocrinol Metab 90 (2005) 789-794
45. Shepherd R.M., Cosgrove K.E., O'Brien R.E., Barnes P.D., Ammala C., and Dunne M.J. Hyperinsulinism of infancy: towards an understanding of unregulated insulin release. European Network for Research into Hyperinsulinism in Infancy. Arch Dis Child Fetal Neonatal Ed 82 (2000) 87-97
46. Dunne M.J., Cosgrove K.E., Shepherd R.M., Aynsley-Green A., and Lindley K.J. Hyperinsulinism in infancy: from basic science to clinical disease. Physiol Rev 84 (2004) 239-275
47. Geng X., Li L., Watkins S., Robbins P.D., and Drain P. The insulin secretory granule is the major site of K-ATP channels of the endocrine pancreas. Diabetes 52 (2003) 767-776
48. Thornton P.S., MacMullen C., Ganguly A., et al. Clinical and molecular characterization of a dominant form of congenital hyperinsulinism caused by a mutation in the high-affinity sulfonylurea receptor. Diabetes 52 (2003) 2403-2410
49. Tornovsky S., Crame A., Hussain K., et al. Hyperinsulinism of infancy: novel ABCC8 and KCNJ11 mutations and evidence for additional locus heterogeneity. J Clin Endocrinol Metab 89 (2004) 6224-6234
50. Fournet J.C., Mayaud C., de Lonlay P., et al. Loss of imprinted genes and paternal SUR1 mutations lead to focal form of congenital hyperinsulinism. Horm Res 53 Suppl 1 (2000) 2-6
51. Verkarre V., Fournet J.C., de Lonlay P., et al. Paternal mutation of the sulfonylurea receptor (SUR1) gene and maternal loss of 11p15 imprinted genes lead to persistent hyperinsulinism in focal adenomatous hyperplasia. J Clin Invest 102 (1998) 1286-1291
52. Fournet J.C., Mayaud C., deLonlay P., et al. Unbalanced expression of 11p15 imprinted genes in focal forms of congenital hyperinsulinism: association with a reduction to homozygosity of a mutation in ABCC8 or KCNJ11. Am J Pathol 158 (2001) 2177-2184
53. Glaser B., Kasevan P., Heyman M., et al. Familial hyperinsulinism caused by an activating glucokinase mutation. N Engl J Med 338 (1998) 226-230
54. Cuesta-Munoz A.L., Houpio H., Otonkoski T., et al. Severe persistent hyperinsulinemic hypoglycemia due to a de novo glucokinase mutation. Diabetes 53 (2004) 2164-2168
55. MacMullen C.., Fang J., Hsu B.Y., et al. Hyperinsulinism/hyperammonemia syndrome in children with regulatory mutations in the inhibitory guanosine triphosphate-binding domain of glutamate dehydrogenase. J Clin Endocrinol Metab 86 (2001) 1782-1787
56. Stanley C.A., Lieu Y.K., Hsu B.Y., et al. Hyperinsulinism and hyperammonemia in infants with regulatory mutations of the glutamate dehydrogenase gene. N Engl J Med 338 (1998) 1352-1357
57. Stanley C.A., Fang J., Kutyna K., et al. Molecular basis and characterization of the hyperinsulinism/hyperammonemia syndrome: predominance of mutations in exons 11 and 12 of the glutamate dehydrogenase gene. HI/HA Contributing Investigators. Diabetes 49 (2000) 667-673
58. de Lonlay P., Simon-Carre A., Ribeiro M.J., et al. Congenital hyperinsulinism: pancreatic [18F]fluoro-l-dihydroxyphenylalanine (DOPA) positron emission tomography and immunohistochemistry study of DOPA decarboxylase and insulin secretion. J Clin Endocrinol Metab 91 (2006) 933-940
59. Otonkoski T., Näntö-Salonen K., Seppanen M., et al. Noninvasive diagnosis of focal hyperinsulinism of infancy with [18F]-DOPA positron emission tomography. Diabetes 55 (2006) 13-18
60. Mohnike K., Blankenstein O., Christesen H.T., et al. Proposal for a standardized protocol for 18F-DOPA-PET (PET/CT) in congenital hyperinsulinism. Horm Res 66 (2006) 43-44
61. Kassem S.A., Ariel I., Thornton P.S., et al. p57-KIP2 expression in normal islets cells and in hyperinsulinism of infancy. Diabetes 50 (2001) 2763-2769
62. Potikha T., Kassem S., Haber E.P., Ariel I., and Glaser B. p57Kip2 (cdkn1c): sequence, splice variants and unique temporal and spatial expression pattern in the rat pancreas. Lab Invest 85 (2005) 364-375
63. Dunne M.J., Kane C., Shepherd R.M., et al. Familial persistent hyperinsulinemic hypoglycemia of infancy and mutations in the sulfonylurea receptor. N Engl J Med 336 (1997) 703-706
64. Glaser B., Phillip M., Carmi R., Lieberman E., and Landau H. Persistent hyperinsulinemic hypoglycemia of infancy ("nesidioblastosis"): autosomal recessive inheritance in 7 pedigrees. Am J Med Genet 37 (1990) 511-515
65. Thornton P.S., Satin-Smith M.S., Herold K., et al. Familial hyperinsulinism with apparent autosomal dominant inheritance: clinical and genetic differences from the autosomal recessive variant. J Pediatr 132 (1998) 9-14
66. de Lonlay P., Giurgea I., Sempoux C., et al. Dominantly inherited hyperinsulinaemic hypoglycaemia. J Inherit Metab Dis 28 (2005) 267-276
67. Nestorowicz A., Inagaki N., Gonoi T., et al. A nonsense mutation in the inward rectifier potassium channel gene, Kir6.2, is associated with familial hyperinsulinism. Diabetes 46 (1997) 1743-1748
68. Lin Y.W., MacMullen C., Ganguly A., Stanley C.A., and Shyng S.L. A novel KCNJ11 mutation associated with congenital hyperinsulinism reduces the intrinsic open probability of beta-cell ATP-sensitive potassium channels. J Biol Chem 281 (2006) 3001-3012
69. Kane C., Lindley K.J., Johnson P.R., et al. Therapy for persistent hyperinsulinemic hypoglycemia of infancy. Understanding the responsiveness of beta cells to diazoxide and somatostatin. J Clin Invest 100 (1997) 1888-1893