Skip to main content

Advertisement

SpringerLink
Log in

Gastrointestinal neuromuscular pathology: guidelines for histological techniques and reporting on behalf of the Gastro 2009 International Working Group

  • Consensus Paper
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Abstract

The term gastrointestinal neuromuscular disease describes a clinically heterogeneous group of disorders of children and adults in which symptoms are presumed or proven to arise as a result of neuromuscular, including interstitial cell of Cajal, dysfunction. Such disorders commonly have impaired motor activity, i.e. slowed or obstructed transit with radiological evidence of transient or persistent visceral dilatation. Whilst sensorimotor abnormalities have been demonstrated by a variety of methods in these conditions, standards for histopathological reporting remain relatively neglected. Significant differences in methodologies and expertise continue to confound the reliable delineation of normality and specificity of particular pathological changes for disease. Such issues require urgent clarification to standardize acquisition and handling of tissue specimens, interpretation of findings and make informed decisions on risk-benefit of full-thickness tissue biopsy of bowel or other diagnostic procedures. Such information will also allow increased certainty of diagnosis, facilitating factual discussion between patients and caregivers, as well as giving prognostic and therapeutic information. The following report, produced by an international working group, using established consensus methodology, presents proposed guidelines on histological techniques and reporting for adult and paediatric gastrointestinal neuromuscular pathology. The report addresses the main areas of histopathological practice as confronted by the pathologist, including suction rectal biopsy and full-thickness tissue obtained with diagnostic or therapeutic intent. For each, indications, safe acquisition of tissue, histological techniques, reporting and referral recommendations are presented.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

AChE:

Acetylcholinesterase

CIPO:

Chronic intestinal pseudo-obstruction

GINMD:

Gastrointestinal neuromuscular disease

GINMP:

Gastrointestinal neuromuscular pathology

H&E:

Haematoxylin and eosin

HSCR:

Hirschsprung disease

IBS:

Irritable bowel syndrome

ICC:

Interstitial cells of Cajal

IELs:

Intraepithelial lymphocytes

IHC:

Immunohistochemistry

IND:

Intestinal neuronal dysplasia

IWG:

International working group

NOTES:

Natural orifice transluminal endoscopic surgery

NSE:

Neuron specific enolase

PAS:

Periodic acid-Schiff

PGP 9.5:

Protein gene product 9.5

SRB:

Suction rectal biopsy

TEM:

Transmission electron microscopy

References

  1. Akbar A, Yiangou Y, Facer P, Walters JR, Anand P, Ghosh S (2008) Increased capsaicin receptor TRPV1 expressing sensory fibres in irritable bowel syndrome and their correlation with abdominal pain. Gut 57:923–929. doi:10.1136/gut.2007.138982

    PubMed  CAS  Google Scholar 

  2. Aldridge RT, Campbell PE (1968) Ganglion cell distribution in the normal rectum and anal canal. A basis for the diagnosis of Hirschsprung’s disease by anorectal biopsy. J Pediatr Surg 3:475–489. doi:10.1016/0022-3468(68)90670-2

    PubMed  CAS  Google Scholar 

  3. Alizai NK, Batcup G, Dixon MF, Stringer MD (1998) Rectal biopsy for Hirschsprung’s disease: what is the optimum method. Pediatr Surg Int 13:121–124. doi:10.1007/s003830050264

    PubMed  CAS  Google Scholar 

  4. Arista Nasr J, Gonzalez-Romo M, Keirns C, Larriva-Sahd J (1993) Diffuse lymphocytic infiltration of the small intestine with damage to the nerve plexus. Arch Pathol Lab Med 117:812–819

    PubMed  CAS  Google Scholar 

  5. Ariza A, Coll J, Fernandez-Figueras MT et al (1995) Desmin myopathy: a multisystem disorder involving skeletal, cardiac and smooth muscle. Hum Pathol 26:1032–1037. doi:10.1016/0046-8177(95)90095-0

    PubMed  CAS  Google Scholar 

  6. Athow AC, Filipe MI, Drake DP (1990) Problems and advantages of acetylcholinesterase histochemistry of rectal suction biopsies in the diagnosis of Hirschsprung’s disease. J Pediatr Surg 25:520–526. doi:10.1016/0022-3468(90)90564-P

    PubMed  CAS  Google Scholar 

  7. Attwood SE, Kelly I, O’Connell PR, Corrigan T (1993) Laparoscopic mobilization and exteriorization for minimally invasive small bowel resection. Br J Surg 80:225. doi:10.1002/bjs.1800800235

    PubMed  CAS  Google Scholar 

  8. Barbara G, De Giorgio R, Stanghellini V, Cremon C, Corinaldesi R (2002) A role for inflammation in irritable bowel syndrome? Gut 51(Suppl 1):i41–i44. doi:10.1136/gut.51.suppl_1.i41

    PubMed  Google Scholar 

  9. Barbara G, Stanghellini V, De Giorgio R, Cremon C, Cottrell GS, Santini D et al (2004) Activated mast cells in proximity to olonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 126:693–702. doi:10.1053/j.gastro.2003.11.055

    PubMed  Google Scholar 

  10. Barbara G, Wang B, Stanghellini V, De Giorgio R, Cremon C, Di Nardo G et al (2007) Mast cell-dependent excitation of visceral nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology 132:26–37. doi:10.1053/j.gastro.2006.11.039

    PubMed  CAS  Google Scholar 

  11. Barnett JL, McDonnell WM, Appelman HD, Dobbins WO (2004) Familial visceral neuropathy with neuronal intranuclear inclusions: diagnosis by rectal biopsy. Gastroenterology 102:684–691

    Google Scholar 

  12. Barshack I, Fridman E, Goldberg I, Chowers Y, Koplovic J (2004) The loss of calretinin expression indicates aganglionosis in Hirschsprung’s disease. J Clin Pathol 57:712–716. doi:10.1136/jcp.2004.016030

    PubMed  CAS  Google Scholar 

  13. Bassotti G, Villanacci V, Cathomas G, Maurer CA, Fisogni S, Cadei M (2006) Enteric neuropathology of the terminal ileum in patients with intractable slow-transit constipation. Hum Pathol 37:1252–1258. doi:10.1016/j.humpath.2006.04.027

    PubMed  Google Scholar 

  14. Boman F, Sfeir R, Priso R, Bonnevalle M, Besson R (2007) Advantages of intraoperative semiquantitative evaluation of myenteric nervous plexuses in patients with Hirschsprung disease. J Pediatr Surg 42:1089–1094. doi:10.1016/j.jpedsurg.2007.01.052

    PubMed  Google Scholar 

  15. Borchard F, Meier-Ruge W, Wiebecke B et al (1991) Innervationsstörungen des Dickdarms–Klassifikation und Diagnostik. Pathologe 12:171–174

    PubMed  CAS  Google Scholar 

  16. Brittingham J, Phiel C, Trzyna WC, Gabbeta V, McHugh KM (1998) Identification of distinct molecular phenotypes in cultured gastrointestinal smooth muscle cells. Gastroenterology 115:605–617. doi:10.1016/S0016-5085(98)70140-4

    PubMed  CAS  Google Scholar 

  17. Bruder E, Knecht Y, Kasper M, Chaffard R, Ipsen S, Terracciano L et al (2007) Enzyme histochemical diagnosis of gastrointestinal motility disorders. A Laboratory guide. Pathologie 28:93–100. doi:10.1007/s00292-007-0902-1

    CAS  Google Scholar 

  18. Bughaighis AG, Emery JL (1971) Functional obstruction of the intestine due to neurological immaturity. Prog Pediatr Surg 3:37–52

    PubMed  CAS  Google Scholar 

  19. Camilleri M, Cowen T, Koch TR (2008) Enteric neurodegeneration in ageing. Neurogastroenterol Motil 20:418–429. doi:10.1111/j.1365-2982.2008.01134.x

    PubMed  CAS  Google Scholar 

  20. Cellek S, Foxwell NA, Moncada S (2003) Two phases of nitrergic neuropathy in streptozotocin-induced diabetic rats. Diabetes 52:2353–2362. doi:10.2337/diabetes.52.9.2353

    PubMed  CAS  Google Scholar 

  21. Chadwick VS, Chen W, Shu D, Paulus B, Bethwaite P, Tie A et al (2002) Activation of the mucosal immune system in irritable bowel syndrome. Gastroenterology 122:1778–1783. doi:10.1053/gast.2002.33579

    PubMed  Google Scholar 

  22. Chang F, Mahadeva U, Deere H (2005) Pathological and clinical significance of increased intraepithelial lymphocytes (IELs) in small bowel mucosa. APMIS 113:385–399. doi:10.1111/j.1600-0463.2005.apm_204.x

    PubMed  Google Scholar 

  23. Clark SB, Rice TW, Tubbs RR, Richter JE, Goldblum JR (2000) The nature of the myenteric infiltrate in achalasia: an immunohistochemical analysis. Am J Surg Pathol 24:1153–1158. doi:10.1097/00000478-200008000-00014

    PubMed  CAS  Google Scholar 

  24. Coerdt W, Michel J-S, Rippin G et al (2004) Quantitative morphometric analysis of the submucous plexus in age-related control groups. Virchows Arch 444:239–246. doi:10.1007/s00428-003-0951-7

    PubMed  Google Scholar 

  25. Cord-Udy C, Smith VV, Ahmed S, Milla PJ, Risdon RA (1997) An evaluation of the role of suction rectal biopsy in the diagnosis of intestinal neuronal dysplasia. J Pediatr Gastroenterol Nutr 24:1–6. doi:10.1097/00005176-199701000-00002

    PubMed  CAS  Google Scholar 

  26. Csendes A, Smok G, Braghetto I et al (1992) Histological studies of Auerbach’ plexuses of the oesophagus, stomach, jejunum, and colon in patients with achalasia of the oesophagus: correlation with gastric acid secretion, presence of parietal cells and gastric emptying of solids. Gut 33:150–154. doi:10.1136/gut.33.2.150

    PubMed  CAS  Google Scholar 

  27. Danesh BJZ, Burke M, Newman J, Aylott A, Whitfield P, Cotton PR (1985) Comparison of weight, depth and diagnostic adequacy of specimens obtained with 16 different biopsy forceps designed for upper gastrointestinal endoscopy. Gut 26:227–231. doi:10.1136/gut.26.3.227

    PubMed  CAS  Google Scholar 

  28. De Giorgio R, Barbara G (2008) Is irritable bowel syndrome an inflammatory disorder? Curr Gastroenterol Rep 10:385–390. doi:10.1007/s11894-008-0073-0

    PubMed  Google Scholar 

  29. De Giorgio R, Barbara G, Stanghellini V, Cogliandro RF, Arrigoni A, Santini D (2000) Idiopathic myenteric ganglionitis underlying intractable vomiting in a young adult. Eur J Gastroenterol Hepatol 12:613–616. doi:10.1097/00042737-200012060-00006

    PubMed  Google Scholar 

  30. De Giorgio R, Barbara G, Stanghellini V, De Ponti F, Salvioli B, Tonini M et al (2002) Clinical and morphofunctional features of idiopathic myenteric ganglionitis underlying severe intestinal motor dysfunction: a study of three cases. Am J Gastroenterol 97:2454–2459. doi:10.1016/S0002-9270(02)04359-9

    PubMed  Google Scholar 

  31. De Giorgio R, Guerrini S, Barbara G, Cremon C, Stanghellini V, Corinaldesi R (2004) New insights into human enteric neuropathies. Neurogastroenterol Motil 16(suppl 1):143–147. doi:10.1111/j.1743-3150.2004.00491.x

    PubMed  Google Scholar 

  32. De Giorgio R, Sarnelli G, Corinaldesi R, Stanghellini V (2004) Advance in our understanding of the pathology of chronic intestinal pseudo-obstruction. Gut 53:1549–1552. doi:10.1136/gut.2004.043968

    PubMed  Google Scholar 

  33. DeSchryver-Kecskemeti K, Clouse RE (1989) Perineural and intraneural inflammatory infiltrates in the intestines of patients with systemic connective-tissue disease. Arch Pathol Lab Med 113:394–398

    PubMed  CAS  Google Scholar 

  34. de Souza RR, Moratelli HB, Borges N, Liberti EA (1993) Age-induced nerve cell loss in the myenteric plexus of the small intestine in man. Gerontology 39:183–188

    Article  PubMed  Google Scholar 

  35. Dobbins WO, Bill AH (1965) Diagnosis of Hirschsprung’s disease excluded by rectal suction biopsy. N Engl J Med 272:990–993

    PubMed  Google Scholar 

  36. Drossman DA (2007) Introduction. The Rome Foundation and Rome III. Neurogastroenterol Motil 19:783–786. doi:10.1111/j.1365-2982.2007.01001.x

    PubMed  CAS  Google Scholar 

  37. Duchen LW, Anjorin A, Watkins PJ, Mackay JD (1980) Pathology of autonomic neuropathy in diabetes mellitus. Ann Intern Med 92:301–303

    PubMed  CAS  Google Scholar 

  38. Dvorak AM, Onderdonk AB, McLeod RS et al (1993) Axonal necrosis of enteric autonomic nerves in continent ileal pouches. Possible implications for pathogenesis of Crohn’s disease. Ann Surg 217:260–271. doi:10.1097/00000658-199303000-00008

    PubMed  CAS  Google Scholar 

  39. Dvorak AM, Osage JE, Monahan RA, Dickersin GR (1980) Crohns’s disease: transmission electron microscopic studies. III. Target tissues. Proliferation and injury to smooth muscle cells and the autonomic nervous system. Hum Pathol 11:620–634. doi:10.1016/S0046-8177(80)80073-6

    PubMed  CAS  Google Scholar 

  40. Dyer NH, Dawson AM, Smith BF, Todd IP (1969) Obstruction of the bowel due to a lesion in the myenteric plexus. BMJ I:686–689

    Google Scholar 

  41. Ehrenpreis T (1966) Seminar on Pseudo-Hirschsprung’s disease and related disorders. Arch Dis Child 41:143–154. doi:10.1136/adc.41.216.137

    Google Scholar 

  42. Ellison D, Love S, Chimelli L et al (1998) Neuropathology. A reference text of CNS pathology. C. V. Mosby Co., St. Louis, pp 1.1–1.18

    Google Scholar 

  43. Eltringham WK, Roe AM, Galloway SW et al (1993) A laparoscopic technique for full-thickness intestinal biopsy and feeding jejunostomy. Gut 34:122–124. doi:10.1136/gut.34.1.122

    PubMed  CAS  Google Scholar 

  44. Emery JL (1973) Colonic retention syndrome (megacolon) associated with immaturity of intestinal intramural plexus. Proc R Soc Med 66:222–223

    PubMed  CAS  Google Scholar 

  45. Erdohazi M (1974) Retarded development of the enteric myenteric plexus. Dev Med Child Neurol 16:365–368

    PubMed  CAS  Google Scholar 

  46. Espinosa I, Lee CH, Kim MK, Rouse BT, Subramanian S, Montomery K et al (2008) A novel monoclonal antibody against DOG1 is a sensitive and specific marker for gastrointestinal stromal tumors. Am J Surg Pathol 32:210–218. doi:10.1097/PAS.0b013e3181238cec

    PubMed  Google Scholar 

  47. Facer P, Knowles CH, Thomas PK, Tam PK, Williams NS, Anand P (2001) Decreased tyrosine kinase C expression may reflect developmental abnormalities in Hirschsprung’s disease and idiopathic slow-transit constipation. Br J Surg 88:545–552. doi:10.1046/j.1365-2168.2001.01731.x

    PubMed  CAS  Google Scholar 

  48. Farrugia G (2008) Interstitial cells of Cajal in health and disease. Neurogastroenterol Motil 20(Suppl 1):54–63. doi:10.1111/j.1365-2982.2008.01109.x

    PubMed  Google Scholar 

  49. Faussone-Pellegrini MS, Fociani P, Buffa R, Basilisco G (1999) Loss of interstitial cells and a fibromuscular layer on the luminal side of the colonic circular muscle presenting a megacolon in an adult patient. Gut 45:775–779

    PubMed  CAS  Google Scholar 

  50. Fitzgibbons PL, Chandrasoma PT (1987) Familial visceral myopathy. Evidence of diffuse involvement of intestinal smooth muscle. Am J Surg Pathol 11:846–854. doi:10.1097/00000478-198711000-00003

    PubMed  CAS  Google Scholar 

  51. Forster J, Damjanov I, Lin Z, Sarosiek I, Wetzel P, McCallum RW (2005) Absence of the interstitial cells of Cajal in patients with gastroparesis and correlation with clinical findings. J Gastrointest Surg 9:102–108. doi:10.1016/j.gassur.2004.10.001

    PubMed  Google Scholar 

  52. Gabella G (1981) Structure of muscles and nerves in the gastrointestinal tract. In: Johnson LR (ed) Physiology of the Gastrointestinal tract, Chap 6. Raven Press, New York, pp 197–241

    Google Scholar 

  53. Ganns D, Schrödl F, Neuhuber W, Brehmer A (2006) Investigation of general and cytoskeletal markers to estimate numbers and proportions of neurons in the human intestine. Histol Histopathol 21:41–51

    PubMed  CAS  Google Scholar 

  54. Gattuso JM, Kamm MA (1997) Clinical features of idiopathic megarectum and idiopathic megacolon. Gut 41:93–99

    PubMed  CAS  Google Scholar 

  55. Gattuso JM, Smith VV, Kamm MA (1998) Altered contractile proteins and neural innervation in idiopathic megarectum and megacolon. Histopathology 33:34–38. doi:10.1046/j.1365-2559.1998.00438.x

    PubMed  CAS  Google Scholar 

  56. Giniès JL, François H, Joseph MG, Champion G, Coupris L, Limal JM (1996) A curable cause of chronic idiopathic intestinal pseudo-obstruction in children: idiopathic myositis of the small intestine. J Pediatr Gastroenterol Nutr 23:426–429. doi:10.1097/00005176-199611000-00012

    PubMed  Google Scholar 

  57. Gladman MA, Knowles CH (2008) Novel concepts in the diagnosis, pathophysiology and management of idiopathic megabowel. Colorectal Dis 10:531–538. doi:10.1111/j.1463-1318.2007.01457.x

    PubMed  CAS  Google Scholar 

  58. Gladman MA, Knowles CH (2008) Surgical treatment of patients with constipation and fecal incontinence. Gastroenterol Clin North Am 37:605–625. doi:10.1016/j.gtc.2008.06.009

    PubMed  Google Scholar 

  59. Glia A (1999) Immunohistochemical studies of the small bowel and the colon in patients with slow transit constipation. In: Glia A (ed) Constipation: symptoms and findings in relation to structural and functional abnormalities. Karolinska Institutet, Stockholm. http://diss.kib.ki.se/1999/91-628-3379-0/

  60. Greig JD, Miles WF, Nixon SJ (1995) Laparoscopic technique for small bowel biopsy. Br J Surg 82:363. doi:10.1002/bjs.1800820326

    PubMed  CAS  Google Scholar 

  61. Haas S, Bindl L, Fischer HP (2005) Autoimmune enteric leiomyositis: a rare cause of chronic intestinal pseudo-obstruction with specific morphological features. Hum Pathol 36:576–580. doi:10.1016/j.humpath.2005.01.005

    PubMed  Google Scholar 

  62. Hayat M, Cairns A, Dixon MF, O’Mahony S (2002) Quantitation of intraepithelial lymphocytes in human duodenum: what is normal? J Clin Pathol 55:393–394

    PubMed  CAS  Google Scholar 

  63. He C-L, Burgart L, Wang L et al (2000) Decreased interstitial cell of Cajal volume in patients with slow-transit constipation. Gastroenterology 118:14–21. doi:10.1016/S0016-5085(00)70409-4

    PubMed  CAS  Google Scholar 

  64. Heneyke S, Smith VV, Spitz L, Milla PJ (1999) Chronic intestinal pseudo-obstruction: treatment and long term follow-up of 44 patients. Arch Dis Child 81:21–27. doi:10.1136/adc.81.1.21

    PubMed  CAS  Google Scholar 

  65. Herrera GA, Pinto de Moraes H, Grizzle WE, Han SG (1984) Malignant small bowel neoplasm of enteric plexus derivation (plexosarcoma). Light and electron microscopic study confirming the origin of the neoplasm. Dig Dis Sci 29:275–284. doi:10.1007/BF01296263

    PubMed  CAS  Google Scholar 

  66. Hiatt RB, Katz L (1962) Mast cells in inflammatory conditions of the gastrointestinal tract. Am J Gastroenterol 37:541–545

    PubMed  CAS  Google Scholar 

  67. Ho YH, Tan M, Eu KW, Leong A, Choen FS (1997) Laparoscopic-assisted compared with open total colectomy in treating slow transit constipation. Aust N Z J Surg 67:562–565. doi:10.1111/j.1445-2197.1997.tb02039.x

    PubMed  CAS  Google Scholar 

  68. Hoff S, Zeller F, von Weyhern CW, Wegner M, Schemann M, Michel K et al (2008) Quantitative assessment of glial cells in the human and guinea pig enteric nervous system with an anti-Sox8/9/10 antibody. J Comp Neurol 509:356–371. doi:10.1002/cne.21769

    PubMed  Google Scholar 

  69. Holschneider AM, Meier-Ruge W, Ure BM (1994) Hirschsprung’s disease and allied disorders–a review. Eur J Pediatr Surg 4:260–266. doi:10.1055/s-2008-1066115

    PubMed  CAS  Google Scholar 

  70. Hubball A, Martin JE, Lang B, De Giorgio R, Knowles CH (2008) The role of humoral autoimmunity in gastrointestinal neuromuscular diseases. Prog Neurobiol (in press)

  71. Hutson JM, Chow CW, Borg J (1996) Intractable constipation with a decrease in Substance P-immunoreactive fibres: is it a variant of intestinal neuronal dysplasia? J Ped Surg 31:580–583. doi:10.1016/S0022-3468(96)90501-1

    CAS  Google Scholar 

  72. Isozaki K, Hirota S, Miyagawa J, Taniguchi M, Shinomura Y, Matsuzawa Y (1997) Deficiency of c-kit + cells in patients with a myopathic form of chronic idiopathic intestinal pseudo-obstruction. Am J Gastroenterol 92:332–334

    PubMed  CAS  Google Scholar 

  73. Iwasaki H, Kajimura M, Osawa S, Kanaoka S, Furuta T, Ikuma M et al (2006) A deficiency of gastric interstitial cells of Cajal accompanied by decreased expression of neuronal nitric oxide synthase and substance P in patients with type 2 diabetes mellitus. J Gastroenterol 41:1076–1087. doi:10.1007/s00535-006-1909-8

    PubMed  CAS  Google Scholar 

  74. Jacobs E, Ardichvili D, Perissino A, Gottignies P, Hanssens JF (1979) A case of familial visceral myopathy with atrophy and fibrosis of the longitudinal muscle layer of the entire small bowel. Gastroenterology 77:745–750

    PubMed  CAS  Google Scholar 

  75. Jenkins D, Goodall A, Drew K, Scott BB (1988) What is colitis? Statistical approach to distinguishing clinically important inflammatory change in rectal biopsy specimens. J Clin Pathol 41:72–79. doi:10.1136/jcp.41.1.72

    PubMed  CAS  Google Scholar 

  76. Kamiya S, Suzuki Y, Sugimura M (1983) Polyglucosan bodies in the digestive tract of the aged dog. Acta Neuropathol 60:297–300. doi:10.1007/BF00691880

    PubMed  CAS  Google Scholar 

  77. Kapur RP (2003) Neuronal dysplasia: a controversial pathological correlate of intestinal pseudo-obstruction. Am J Med Genet 122A:287–293. doi:10.1002/ajmg.a.20470

    PubMed  Google Scholar 

  78. Kapur RP (2006) Can we stop looking? Immunohistochemistry and the diagnosis of Hirschsprung disease. Am J Clin Pathol 126:9–12. doi:10.1309/T7REY1N43FML7AA8

    PubMed  CAS  Google Scholar 

  79. Kapur RP, de Sa DJ, Luquette M, Jaffe R (1995) Hypothesis: pathogenesis of skip areas in long-segment Hirschsprung’s disease. Pediatr Pathol Lab Med 15:23–37

    PubMed  CAS  Google Scholar 

  80. Kapur RP, Reed RC, Finn L, Patterson K, Johanson J, Rutledge JC (2008) Calretinin immunohistochemistry versus acetylcholinesterase histochemistry in the evaluation of suction rectal biopsies for Hirschsprung disease. Pediatr Dev Pathol (in press)

  81. Kashyap P, Farrugia G (2008) Enteric autoantibodies and gut motility disorders. Gastroenterol Clin North Am 37:397–410. doi:10.1016/j.gtc.2008.02.005

    PubMed  Google Scholar 

  82. Kenny SE, Vanderwinden JM, Rintala RJ, Connell MG, Lloyd DA, Vanderhaeghen JJ et al (1998) Delayed maturation of the interstitial cells of Cajal: a new diagnosis for transient neonatal pseudoobstruction. Report of two cases. J Pediatr Surg 33:94–98. doi:10.1016/S0022-3468(98)90370-0

    PubMed  CAS  Google Scholar 

  83. King PH, Redden D, Palmgren JS, Nabors LB, Lennon VA (1999) Hu antigen specificities of ANNA-1 autoantibodies in paraneoplastic neurological disease. J Autoimmun 13:435–443. doi:10.1006/jaut.1999.0337

    PubMed  CAS  Google Scholar 

  84. King SK, Sutcliffe JR, Hutson JM (2005) Laparoscopic seromuscular colonic biopsies: a surgeon’s experience. J Ped Surg 40:381–384. doi:10.1016/j.jpedsurg.2004.10.031

    Google Scholar 

  85. Knowles CH (2007) New horizons in the pathogenesis of gastrointestinal neuromuscular disease. J Pediatr Gastroenterol Nutr 45(Suppl 2):S97–S102. doi:10.1097/MPG.0b013e31812e6569

    PubMed  Google Scholar 

  86. Knowles CH, De Giorgio R (2008) Observations on a vestigial organ: a potential surrogate for enteric neuromesenchymal disease. Neurogastroenterol Motil 20:263–268. doi:10.1111/j.1365-2982.2008.01090.x

    PubMed  CAS  Google Scholar 

  87. Knowles CH, Martin JE (2000) Slow transit constipation: a model of human gut dysmotility. Review of possible aetiologies. Neurogastroenterol Motil 12:181–196. doi:10.1046/j.1365-2982.2000.00198.x

    PubMed  CAS  Google Scholar 

  88. Knowles CH, Nickols CD, Feakins R, Martin JE (2003) A systematic analysis of polyglucosan bodies in the human gastrointestinal tract in health and disease. Acta Neuropathol 105:410–413

    PubMed  CAS  Google Scholar 

  89. Knowles CH, Nickols CD, Scott SM, Bennett NI, de Oliveira RB, Chimelli L et al (2001) Secondary smooth muscle degeneration with inclusion bodies in slow transit constipation. J Pathol 193:390–397. doi:10.1002/1096-9896(2000)9999:9999<::AID-PATH797>3.0.CO;2-C

    PubMed  CAS  Google Scholar 

  90. Knowles CH, Scott M, Lunniss PJ (1999) Outcome of colectomy for slow transit constipation. Ann Surg 230:627–638. doi:10.1097/00000658-199911000-00004

    PubMed  CAS  Google Scholar 

  91. Knowles CH, Silk DBA, Darzi A, Feakins R, Raimundo AH, Veress B et al (2004) Deranged smooth muscle alpha-actin: a biomarker of intestinal pseudo-obstruction. A controlled multinational case series. Gut 53:1583–1589. doi:10.1136/gut.2003.037275

    PubMed  CAS  Google Scholar 

  92. Knowles CH, Veress B, Tornblom H, Wallace S, Paraskevas P, Darzi A (2008) Safety and diagnostic yield of laparoscopically assisted full-thickness bowel biopsy. Neurogastroenterol Motil 20:774–779. doi:10.1111/j.1365-2982.2008.01099.x

    PubMed  CAS  Google Scholar 

  93. Koletzko S, Jesch I, Faus-Kebetaler T, Briner J, Meier-Ruge WA, Muntefering H et al (1999) Rectal biopsy for diagnosis of intestinal neuronal dysplasia in children: a prospective multicentre study on interobserver variation and clinical outcome. Gut 44:853–861

    Article  PubMed  CAS  Google Scholar 

  94. Krishnamurthy S, Heng Y, Schuffler MD (1993) Chronic intestinal pseudo-obstruction in infants and children caused by diverse abnormalities of the myenteric plexus. Gastroenterology 104:1398–1408

    PubMed  CAS  Google Scholar 

  95. Krishnamurthy S, Schuffler MD (1987) Pathology of neuromuscular disorders of the small intestine and colon. Gastroenterology 93:610–639

    PubMed  CAS  Google Scholar 

  96. Krishmanurthy S, Schuffler MD, Rohrmann CA, Pope CEII (1985) Severe idiopathic constipation is associated with a distinctive abnormality of the colonic myenteric plexus. Gastroenterology 88:26–34

    Google Scholar 

  97. Kulikova-Schupak R, Knupp KG, Pascual JM, Chin SS, Kairam R, Patterson MC (2004) Rectal biopsy in the diagnosis of neuronal intranuclear hyaline inclusion disease. J Child Neurol 19:59–62. doi:10.1177/08830738040190010707

    PubMed  Google Scholar 

  98. Kumar D, Phillips SF (1989) Human myenteric plexus: confirmation of unfamiliar structures in adults and neonates. Gastroenterology 96:1021–1028

    PubMed  CAS  Google Scholar 

  99. Kume M (1971) Personal communication. J Jpn Soc Pediatr Surg 6:479

    Google Scholar 

  100. Lake BD, Puri P, Nixon HH, Claireaux AE (1978) Hirschsprung’s disease: an appraisal of histochemically demonstrated acetylcholinesterase activity in suction rectal biopsy specimens as an aid to diagnosis. Arch Pathol Lab Med 102:244–247

    PubMed  CAS  Google Scholar 

  101. Lazenby AJ, Yardley JH, Giardiello FM, Jessurun J, Bayless TM (1989) Lymphocytic (“microscopic”) colitis: a comparative histopathologic study with particular reference to collagenous colitis. Hum Pathol 20:18–28. doi:10.1016/0046-8177(89)90198-6

    PubMed  CAS  Google Scholar 

  102. Lee J, Ip W, Durie P (1997) Is fibrosing colonopathy an immune mediated disease? Arch Dis Child 77:66–70. doi:10.1136/adc.77.1.66

    PubMed  CAS  Google Scholar 

  103. Liddell RA, Syms M, McHugh KM (1993) Heterogeneous isoactin gene expression in the adult rat gastrointestinal tract. Gastroenterology 105:347–356

    PubMed  CAS  Google Scholar 

  104. Lyford GL HECL, Soffer HE, Hull TL, Strong SA, Senagore AJ et al (2002) Pan-colonic decrease in interstitial cells of Cajal in patients with slow transit constipation. Gut 51:495–496. doi:10.1136/gut.51.4.496

    Google Scholar 

  105. Mainguet P, Jouret A (1996) The collaboration between the endoscopist and the pathologist. Acta Endoscopica 26:67–77. doi:10.1007/BF02965791

    Google Scholar 

  106. Mann SD, Debinski HS, Kamm MA (1997) Clinical characteristics of chronic idiopathic intestinal pseudo-obstruction in adults. Gut 41:675–681

    Article  PubMed  CAS  Google Scholar 

  107. Martin JE, Hester TW, Aslam H, Sinha S, Knowles CH (2008) Discordant practice and limited histopathological assessment in gastrointestinal neuromuscular disease. Gut (submitted)

  108. Martin JE, Smith VV, Domizio P (1999) Myopathies of the gastro-intestinal tract. In: Lowe J, Underwood JC (eds) Recent Advances in Histopathology 18. Churchill Livingstone, Edinburgh, pp 43–62

    Google Scholar 

  109. McDonald GB, Schuffler MD, Kadin ME, Tytgat GNJ (1985) Intestinal pseudoobstruction caused by diffuse lymphoid infiltration of the small intestine. Gastroenterology 89:882–889

    PubMed  CAS  Google Scholar 

  110. Meier-Ruge W (1971) Über en Erkrankungsbild des Colon mit Hirschsprung-symptomatik. Verh Dtsch Ges Pathol 55:506–510

    PubMed  CAS  Google Scholar 

  111. Meier-Ruge W, Bruder E (2005) Pathology of chronic constipation in pediatric and adult coloproctology. Pathobiology 72:1–102

    PubMed  Google Scholar 

  112. Meier-Ruge WA, Bruder E, Kapur RP (2006) Intestinal neuronal dysplasia type B: one giant ganglion is not good enough. Pediatr Dev Pathol 9:444–452. doi:10.2350/06-06-0109.1

    PubMed  Google Scholar 

  113. Meier-Ruge W, Gambazzi F, Käufeler RE, Schmid P, Schmidt CP (1994) The neuropathological diagnosis of neuronal intestinal dysplasia (NID B). Eur J Pediatr Surg 4:267–273. doi:10.1055/s-2008-1066116

    PubMed  CAS  Google Scholar 

  114. Milde P, Guccion JG, Kelly J, Locatelli E, Jones RV (2001) Adult polyglucosan body disease. Arch Pathol Lab Med 125:519–522

    PubMed  CAS  Google Scholar 

  115. Miller SM, Narasimhan RA, Schmalz PF, Soffer EE, Walsh RM, Krishnamurthi V et al (2008) Distribution of interstitial cells of Cajal and nitrergic neurons in normal and diabetic human appendix. Neurogastroenterol Motil 20:349–357. doi:10.1111/j.1365-2982.2007.01040.x

    PubMed  CAS  Google Scholar 

  116. Mitros FA, Schuffler MD, Teja K, Anuras S (1982) Pathologic features of familial visceral myopathy. Hum Pathol 13:825–833. doi:10.1016/S0046-8177(82)80079-8

    PubMed  CAS  Google Scholar 

  117. Moscoso GJ, Driver M, Guy RJ (1986) A form of necrobiosis and atrophy of smooth muscle in diabetic gastric autonomic neuropathy. Pathol Res Pract 181:188–194

    PubMed  CAS  Google Scholar 

  118. National Institute for Health and Clinical Excellence (2007) Making group decisions and reaching consensus. The Guidelines Manual, Chap 9, April, p 58

  119. Navarro J, Sonsino E, Boige N, Nabarra B, Ferkadji L, Mashako LMN et al (1990) Visceral neuropathies responsible for chronic intestinal pseudo-obstruction syndrome in pediatric practice: analysis of 26 cases. J Pediatr Gastroenterol Nutr 11:179–195. doi:10.1097/00005176-199008000-00006

    Article  PubMed  CAS  Google Scholar 

  120. N-Fékété C, Ricour C, Martelli H, Lortat Jacob S, Pelleyin D (1986) Total colonic aganglionosis (with or without ileal involvement): A review of 27 cases. J Pediatr Surg 21:251–254. doi:10.1016/S0022-3468(86)80847-8

    PubMed  Google Scholar 

  121. Ohlsson B, Fork F-T, Veress B, Tóth E (2004) Coexistent chronic idiopathic intestinal pseudo obstruction and inflammatory bowel disease. Gut 54:729–730. doi:10.1136/gut.2004.058826

    Google Scholar 

  122. Ohlsson B, Veress B, Janciauskiene S, Montgomery A, Haglund M, Wallmark A (2007) Chronic intestinal pseudo-obstruction due to buserelin-induced formation of anti-GnRH antibodies. Gastroenterology 132:45–51. doi:10.1053/j.gastro.2006.10.036

    PubMed  CAS  Google Scholar 

  123. O’Kelly TJ, Davies JR, Tam PK, Brading AF, Mortensen NJ (1994) Abnormalities of nitric-oxide-producing neurons in Hirschsprung’s disease: morphology and implications. J Pediatr Surg 29:294–299. doi:10.1016/0022-3468(94)90335-2

    PubMed  Google Scholar 

  124. Park HJ, Kamm MA, Abbasi M, Talbot IC (1995) Immunohistochemical study of the colonic muscle and innervation in idiopathic chronic constipation. Dis Colon Rectum 38:509–513. doi:10.1007/BF02148851

    PubMed  CAS  Google Scholar 

  125. Pasha SF, Lunsford TN, Lennon VA (2006) Autoimmune gastrointestinal dysmotility treated successfully with pyridostigmine. Gastroenterology 131:1592–1596. doi:10.1053/j.gastro.2006.06.018

    PubMed  Google Scholar 

  126. Phillips RJ, Powley TL (2007) Innervation of the gastrointestinal tract: patterns of aging. Auton Neurosci 136:1–19. doi:10.1016/j.autneu.2007.04.005

    PubMed  Google Scholar 

  127. Porter AJ, Wattchow DA, Brookes SJH, Costa M (1997) The neurochemical coding and projections of circular muscle motor neurons in the human colon. Gastroenterology 113:1916–1923. doi:10.1016/S0016-5085(97)70011-8

    PubMed  CAS  Google Scholar 

  128. Porter AJ, Wattchow DA, Hunter A, Costa M (1998) Abnormalities of nerve fibres in the circular muscle of patients with slow transit constipation. Int J Colorectal Dis 13:208–216. doi:10.1007/s003840050163

    PubMed  CAS  Google Scholar 

  129. Preston DM, Butler P, Smith B, Lennard-Jones JE (1984) The neuropathology of slow-transit constipation (abstr). Gut 24:A997

    Google Scholar 

  130. Qualman SJ, Jaffe R, Bove KE, Monforte-Muñoz H (1999) Diagnosis of Hirschsprung’s disease using the rectal biopsy: multi-institutional survey. Pediatr Dev Pathol 2:588–596. doi:10.1007/s100249900167

    PubMed  CAS  Google Scholar 

  131. Quinn FM, Surana R, Puri P (1994) The influence of trisomy 21 on outcome in children with Hirschsprung’s disease. J Pediatr Surg 29:781–783. doi:10.1016/0022-3468(94)90369-7

    PubMed  CAS  Google Scholar 

  132. Rajan E, Gostout CJ, Lurken MS, Talley NJ, Locke GR, Szarka LA et al (2008) Endoscopic “no hole” full-thickness biopsy of the stomach to detect myenteric ganglia. Gastrointest Endosc 67:497–501. doi:10.1016/j.gie.2007.06.024

    PubMed  Google Scholar 

  133. Rudolph CD, Hyman PE, Altschuler SM, Christensen J, Colletti RB, Cucchiara S (1997) Diagnosis and treatment of chronic intestinal pseudo-obstruction in children: report of consensus workshop. J Pediatr Gastroenterol Nutr 24:102–112. doi:10.1097/00005176-199701000-00021

    PubMed  CAS  Google Scholar 

  134. Ruuska TH, Karikoski R, Smith VV, Milla PJ (2002) Acquired myopathic intestinal pseudo-obstruction may be due to autoimmune enteric leiomyositis. Gastroenterology 122:1133–1139

    PubMed  Google Scholar 

  135. Schärli AF, Meier-Ruge W (1981) Localized and disseminated forms of neuronal intestinal dysplasia mimicking Hirschsprung’s disease. J Pediatr Surg 16:164–170. doi:10.1016/S0022-3468(81)80344-2

    PubMed  Google Scholar 

  136. Schuffler MD, Bird TD, Sumi SM, Cook A (1978) A familial neuronal disease presenting as intestinal pseudoobstruction. Gastroenterology 75:889–898

    PubMed  CAS  Google Scholar 

  137. Schuffler MD, Jonak Z (1982) Chronic idiopathic intestinal pseudo-obstruction caused by a degenerative disorder of the myenteric plexus: The use of Smith’s method to define the neuropathology. Gastroenterology 82:476–486

    PubMed  CAS  Google Scholar 

  138. Schuffler MD, Lowe MC, Bill AH (1977) Studies of idiopathic intestinal pseudoobstruction I. Hereditary hollow visceral myopathy: clinical and pathological studies. Gastroenterology 73:327–338

    PubMed  CAS  Google Scholar 

  139. Selgrad M, De Giorgio R, Fini L, Cogliandro RF, Williams S, Stanghellini V et al (2008) JC virus infects the enteric glia of patients with chronic idiopathic intestinal pseudo-obstruction. Gut 14:6717–6721

    CAS  Google Scholar 

  140. Shäppi MG, Smith VV, Milla PJ, Lindley K (2003) Eosinophilic myenteric ganglionitis is associated with functional intestinal obstruction. Gut 52:752–755. doi:10.1136/gut.52.5.752

    Google Scholar 

  141. Sisodia SS (1998) Nuclear inclusions in glutamine repeat disorders: Are they pernicious, coincidental, or beneficial? Cell 95:1–4. doi:10.1016/S0092-8674(00)81743-2

    PubMed  CAS  Google Scholar 

  142. Smith BF (1972) The neuropathology of the alimentary tract. Edward Arnold, London

    Google Scholar 

  143. Smith VV (1993) Neuron density in normal intestine in childhood as a basis for the assessment of hypo and hyperganglionosis. In: Morphological assessment of enteric neuromuscular disease causing intestinal pseudo-obstruction, PhD Thesis, University of London, pp 77-98

  144. Smith VV (1993) Intestinal neuronal density in childhood: a baseline for the objective assessment of hypo- and hyperganglionosis. Pediatr Pathol 13:225–237. doi:10.3109/15513819309048209

    PubMed  CAS  Google Scholar 

  145. Smith VV, Eng C, Milla PJ (1999) Intestinal ganglioneuromatosis and multiple endocrine neoplasia type 2B: implications for treatment. Gut 45:143–146

    Article  PubMed  CAS  Google Scholar 

  146. Smith VV, Gregson N, Foggensteiner L, Neale G, Milla PJ (1997) Acquired intestinal aganglionosis and circulating autoantibodies without neoplasia or other neural involvement. Gastroenterology 112:1366–1371. doi:10.1016/S0016-5085(97)70151-3

    PubMed  CAS  Google Scholar 

  147. Smith VV, Lake BD, Kamm MA, Nicholls JR (1992) Intestinal pseudo-obstruction with deficient smooth muscle alpha actin. Histopathology 21:535–542. doi:10.1111/j.1365-2559.1992.tb00441.x

    PubMed  CAS  Google Scholar 

  148. Smith VV, Milla PJ (1997) Histological phenotypes of enteric smooth muscle disease causing functional intestinal obstruction in childhood. Histopathology 31:112–122. doi:10.1046/j.1365-2559.1997.2250839.x

    PubMed  CAS  Google Scholar 

  149. Smith VV, Schäppi MG, Bisset WM, Kiparissi F, Jaffe A, Milla PJ, et al. (2009) Lymphocytic leiomyositis and myenteric ganglionitis are intrinsic features of cystic fibrosis: studies in distal ileal obstruction syndrome and meconium ileus. J Pediatr Gastroenterol Nutr (in press)

  150. Spiller R, Jenkins D, Thornley J, Hebden J, Wright T, Skinner M et al (2000) Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in post-dysenteric “irritable bowel syndrome”. Gut 47:804–811. doi:10.1136/gut.47.6.804

    PubMed  CAS  Google Scholar 

  151. Streutker C, Huizinga JD, Campbell F, Ho J, Riddell RH (2003) Loss of CD117 (c-kit)- and CD34-positive ICC and associated CD34-positive fibroblasts defines a subpopulation of chronic intestinal pseudo-obstruction. Am J Surg Pathol 27:228–235. doi:10.1097/00000478-200302000-00012

    PubMed  CAS  Google Scholar 

  152. Streutker CJ, Huizinga JD, Driman DK, Riddell RH (2007) Interstitial cells of Cajal in health and disease. Part I: normal ICC structure and function with associated motility disorders. Histopathology 50:176–189. doi:10.1111/j.1365-2559.2006.02493.x

    PubMed  CAS  Google Scholar 

  153. Swenson O, Fisher JH (1959) Hirschsprung’s disease in the newborn. Arch Surg 79:987–993

    PubMed  CAS  Google Scholar 

  154. Tafazzoli K, Soost K, Wessel L, Wedel T (2005) Topographic pecularities of the submucous plexus in the human anorectum–consequences for histopathologic evaluation of rectal biopsies. Eur J Pediatr Surg 15:159–163. doi:10.1055/s-2005-837601

    PubMed  CAS  Google Scholar 

  155. Tanner MS, Smith B, Lloyd JK (1976) Functional intestinal obstruction due to deficiency of argyrophil neurones in the myenteric plexus. Familial syndrome presenting with short small bowel, malrotation, and pyloric hypertrophy. Arch Dis Child 51:837–841. doi:10.1136/adc.51.11.837

    PubMed  CAS  Google Scholar 

  156. Törnblom H, Lindberg G, Nyberg B, Veress B (2002) Full-thickness biopsy of the jejunum reveals inflammation and enteric neuropathy in irritable bowel syndrome. Gastroenterology 123:1972–1979. doi:10.1053/gast.2002.37059

    PubMed  Google Scholar 

  157. Veress B, Franzen L, Bodin L, Borch K (2004) Duodenal intraepithelial lymphocyte-count revisited. Scand J Gastroenterol 39:138–144. doi:10.1080/00365520310007675

    PubMed  CAS  Google Scholar 

  158. Wattchow DA, Porter AJ, Brookes SJH, Costa M (1997) The polarity of neurochemically defined myenteric neurons in the human colon. Gastroenterology 113:497–506. doi:10.1053/gast.1997.v113.pm9247469

    PubMed  CAS  Google Scholar 

  159. Wedel T, Roblick U, Gleiss J, Schiedeck T, Bruch HP, Kühnel W et al (1999) Organization of the enteric nervous system in the human colon demonstrated by wholemount immunohistochemistry with special reference to the submucous plexus. Ann Anat 181:327–337. doi:10.1016/S0940-9602(99)80122-8

    PubMed  CAS  Google Scholar 

  160. Wedel T, Roblick UJ, Ott V, Eggers R, Schiedeck THK, Krammer HJ (2002) Oligoneuronal hypoganglionosis in patients with idiopathic slow transit constipation. Dis Colon Rectum 45:54–62. doi:10.1007/s10350-004-6114-3

    PubMed  CAS  Google Scholar 

  161. Wedel T, Spiegler J, Söllner S, Roblick UJ, Schiedeck THK, Bruch HP et al (2002) Enteric nerves and interstitial cells of Cajal are altered in patients with slow-transit constipation and megacolon. Gastroenterology 123:1459–1467. doi:10.1053/gast.2002.36600

    PubMed  Google Scholar 

  162. Wedel T, van Eys G, Glénisson W, Waltregny D, Vanderwinden JM (2006) Novel smooth muscle markers reveal abnormalities of the intestinal musculature in severe colorectal motility disorders. Neurogastroenterol Motil 18:526–538. doi:10.1111/j.1365-2982.2006.00781.x

    PubMed  CAS  Google Scholar 

  163. White FV, Langer JC (2000) Circumferential distribution of ganglion cells in the transitional zone of children with Hirschsprung disease. Pediatr Dev Pathol 3:216–222. doi:10.1007/s100249910028

    PubMed  CAS  Google Scholar 

  164. Whitehouse FR, Kernohan JW (1948) Myenteric plexus in congenital megacolon; study of 11 cases. Arch Intern Med Chic 82:75–111

    PubMed  CAS  Google Scholar 

  165. Wilder-Smith CH, Talbot IC, Merki HS, Meier-Ruge WA (2002) Morphometric quantification of normal submucous plexus in the distal rectum of adult healthy volunteers. Eur J Gastroenterol Hepatol 14:1339–1342. doi:10.1097/00042737-200212000-00009

    PubMed  Google Scholar 

  166. Wingate D, Hongo M, Kellow J, Lindberg G, Smout A (2002) Disorders of gastrointestinal motility: towards a new classification. J Gastroenterol Hepatol 17(Suppl):S1–S14. doi:10.1046/j.1440-1746.17.s1.7.x

    PubMed  Google Scholar 

  167. Woods KL, Anand BS, Cole RA, Osato MS, Genta RM, Malaty H et al (1999) Influence of endoscopic biopsy forceps characteristics on tissue specimens: results of a prospective randomized study. Gastrointest Endosc 49:177–183. doi:10.1016/S0016-5107(99)70483-9

    PubMed  CAS  Google Scholar 

  168. Yoo SY, Jung SH, Eom M, Kim IH, Han A (2002) Delayed maturation of interstitial cells of Cajal in meconium obstruction. J Pediatr Surg 37:1758–1761. doi:10.1053/jpsu.2002.36715

    PubMed  Google Scholar 

  169. Yoshida MM, Krishnamurthy S, Wattchow DA, Furness JB, Schuffler MD (1988) Megacolon in myotonic dystrophy caused by a degenerative neuropathy of the myenteric plexus. Gastroenterology 95:820–827

    PubMed  CAS  Google Scholar 

  170. Yu CS, Kim HC, Hong HK, Chung DH, Kim HJ, Kang GH et al (2002) Evaluation of myenteric ganglion cells and interstitial cells of Cajal in patients with chronic idiopathic constipation. Int J Colorectal Dis 17:253–258. doi:10.1007/s00384-001-0380-5

    PubMed  Google Scholar 

  171. Yunis EJ, Dibbins AW, Sherman FE (1976) Rectal suction biopsy in the diagnosis of Hirschsprung’s disease. Arch Pathol Lab Med 100:329–333

    PubMed  CAS  Google Scholar 

  172. Zarate N, Wang XY, Tougas G, Anvari M, Birch D, Mearin F et al (2006) Intramuscular interstitial cells of Cajal associated with mast cells survive nitrergic nerves in achalasia. Neurogastroenterol Motil 18:556–568. doi:10.1111/j.1365-2982.2006.00788.x

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This project is supported by an award from Gastro 2009 on behalf of co-operating societies (United European Gastroenterology Federation [UEGF], World Gastroenterology Organization [WGO], British Society of Gastroenterology [BSG], Organisation Mondiale d’Endoscopie Digestive [OMED]). We should also like to thank Professors Colin Rudolph and Jan Huizinga for general guidance, and Doctor Sean Ward for assistance with the ICC section.

Conflict of interest statement

All authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Neurogastroenterology Group, Centres for Academic Surgery and Pathology, Institute of Cellular and Molecular Science, Barts and the London School of Medicine and Dentistry, Queen Mary University London, London, Whitechapel, UK

    Charles H. Knowles & Joanne E. Martin

  2. Department of Clinical Medicine, Alma Mater Studiorum University of Bologna, Bologna, Italy

    Roberto De Giorgio

  3. Department of Pathology, Seattle Children’s Hospital, University of Washington, 4800 Sand Point Way NE, Seattle, WA, 98105, USA

    Raj P. Kapur

  4. Institute of Pathology, University Hospital Basel, Schoenbeinstrasse 40, 4031, Basel, Switzerland

    Elisabeth Bruder & William A. Meier-Ruge

  5. Department of Pathology, University Hospital Zurich, Schmelzbergstrasse 12, 8091, Zurich, Switzerland

    Elisabeth Bruder

  6. Enteric NeuroScience Program, Division of Gastroenterology and Hepatology, Mayo Clinic College of Medicine, 200 First Street SW, Rochester, MN, 55905, USA

    Gianrico Farrugia

  7. Department of Pathology, University Hospital KUL, Minderbroedersstraat 12, 3000, Louvain, Belgium

    Karel Geboes

  8. Anatomy and Cell Biology Faculty, Columbia University Medical Center, 630 West 168th Street, New York, NY, 10032, USA

    Michael D. Gershon

  9. Urology Departments, Royal Children’s Hospital, University of Melbourne and General Surgery, Parkville, VIC, Australia

    John Hutson

  10. Department of Medicine, Karolinska Institutet, Karolinska University Hospital Huddinge, Stockholm, Sweden

    Greger Lindberg

  11. UCL Institute of Child Health, 30 Guilford Street, London, WC1N 1EH, UK

    Peter J. Milla

  12. Department of Histopathology, Camelia Botnar Hospital, Great Ormond Street Hospital NHS Trust, Great Ormond Street, London, WC1N 3JH, UK

    Virpi V. Smith

  13. Laboratory of Neurophysiology, Faculty of Medicine, Université Libre de Bruxelles, route de Lennik 808, 1070, Brussels, Belgium

    Jean Marie Vandervinden

  14. Department of Clinical Pathology and Cytology, University Hospital MAS, Lunds University, Malmö, Sweden

    Béla Veress

  15. Anatomisches Institut, Christian-Albrechts-Universität zu Kiel, Otto-Hahn-Platz 8, 24118, Kiel, Germany

    Thilo Wedel

  16. Centre for Academic Surgery, Royal London Hospital, 3rd Floor Alexandra Wing, London, E1 1BB, UK

    Charles H. Knowles

Authors
  1. Charles H. Knowles
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roberto De Giorgio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Raj P. Kapur
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elisabeth Bruder
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gianrico Farrugia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Karel Geboes
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michael D. Gershon
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. John Hutson
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Greger Lindberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Joanne E. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. William A. Meier-Ruge
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Peter J. Milla
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Virpi V. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jean Marie Vandervinden
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Béla Veress
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Thilo Wedel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Charles H. Knowles.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material (DOC 41 kb)

Supplementary material (PPT 2.01 Mb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Knowles, C.H., De Giorgio, R., Kapur, R.P. et al. Gastrointestinal neuromuscular pathology: guidelines for histological techniques and reporting on behalf of the Gastro 2009 International Working Group. Acta Neuropathol 118, 271–301 (2009). https://doi.org/10.1007/s00401-009-0527-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00401-009-0527-y

Keywords

Search

Navigation