The pathology of neuroendocrine tumours of the gut
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1 The pathology of neuroendocrine tumours of the gut Professor Neil A Shepherd Gloucester & Cheltenham, UK Histopathology Regional Teaching Bristol May
2 The pathology of neuroendocrine tumours (NETs) of the gut: general comments site in the GI tract has a profound influence on the morphology, natural history, hormone elaboration, management & prognosis of NETs grade is an important factor in treatment and prognosis and is an important assessment. This is largely determined by proliferative activity and the Ki67/MIB1 score there is a lack of international conformity about classification with the terms neuroendocrine tumour, endocrine tumour and carcinoid all still being used around the world (WHO and ENETS have different classifications) useful information is available in the Royal College datasets and guidelines at: /G081_DatasetGIEndocrine_Sep12.pdf
3 The clinico-pathological spectrum endocrine cell hyperplasia pure neuro-endocrine cell neoplasms low grade, well differentiated neuro-endocrine tumours (formerly carcinoids) high grade poorly differentiated neuro-endocrine carcinomas (small cell and large cell types) mixed tumours carcinomas of mixed neuro-endocrine and non-endocrine type (MANECs)
4 Markers argentaffin: Masson-Fontana (enterochromaffin cells) argyrophil: Grimelius Churukian-Schenk Sevier-Munger Hellerstrom-Hellman immunohistochemistry in-situ hybridisation
5 Immunostaining cytosol / cell membrane: neurone specific enolase PGP 9.5 CD56, CD99 small vesicle associated markers: synaptophysin SV2 (synaptic vesicle protein 2) secretory granule associated markers: chromogranins A & B Leu-7 (CD57) peptide hormones
6 Upper GI neuro-endocrine tumours well differentiated neuro-endocrine tumour - benign non-functioning, <1 cm, within mucosa-submucosa no angioinvasion well differentiated neuro-endocrine tumour - borderline non-functioning, 1-2 cm, within mucosa-submucosa no angioinvasion well differentiated neuro-endocrine carcinoma any functioning tumour any tumour with angioinvasion or invading beyond submucosa >2 cm poorly differentiated neuro-endocrine carcinoma intermediate or small cell carcinoma
7 Lower GI neuro-endocrine tumours well differentiated neuro-endocrine tumour - benign non-functioning, <2 cm, within mucosa-submucosa, no angioinvasion well differentiated neuro-endocrine tumour - borderline non-functioning, <2 cm, within mucosa-submucosa with angioinvasion well differentiated neuro-endocrine carcinoma any functioning tumour any tumour >2cm or invading beyond submucosa poorly differentiated neuro-endocrine carcinoma intermediate or small cell carcinoma
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9 Pape UF et al. Cancer 2008; 113:
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12 Upper GI tumours Pape UF et al. Cancer 2008; 113:
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14 Oesophageal neuro-endocrine tumours uncommon, usually in distal oesophagus very rare well differentiated NETs arising in a background of Barrett s oesophagus majority are bulky G3 neuro-endocrine carcinomas of small cell type synaptophysin > chromogranin express TTF-1 some are admixed with in situ or invasive squamous or adenocarcinoma (MANEC) Maru D et al. Am J Surg Pathol 2008; 32:
15 Oesophageal NETs prognosis worse for pure neuroendocrine carcinomas than for mixed tumours no difference in survival of pure small cell and large cell Maru D et al. Am J Surg Pathol 2008; 32:
16 Neuro-endocrine cells of the stomach A ghrelin corpus EC serotonin antrum & corpus D somatostatin antrum & corpus ECL histamine corpus X, D1, P endothelin (X) corpus G gastrin antrum
17 Enterochromaffin-like (ECL) cells ~40% of neuro-endocrine cells of gastric corpus mucosa argyrophil but non-argentaffin chromogranin A-positive vesicular granules on electron microscopy contain histamine histidine decarboxylase vesicular monoamine transporter 2 - VMAT-2 secrete histamine in response to gastrin and PACAP (pituitary adenylyl cyclase activating peptides) proliferation induced by hypergastrinaemia
18 ECL-cell tumours in hypergastrinaemia chronic atrophic gastritis (type I) Zollinger-Ellison syndrome (type II) defective parietal cell function (type IV) sporadic ECL-cell (Type III)
19 chronic atrophic gastritis intragastric hypoacidity antral G cells hypergastrinaemia corpus ECL-cell hyperplasia corpus ECL-cell dysplasia corpus ECL-cell neuro-endocrine tumours
20 ECL cell lesions in the stomach hyperplasia simple linear linear sequences of 5 or more cells micronodular 5 or more in clusters <150 µm dysplasia nodules µm, fusion, stromal response invasive neuro-endocrine tumour >500 µm, submucosal invasion
21 Neuroendocrine pathology in chronic atrophic gastritis
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24 Type 1: ECL-cell tumours in chronic atrophic gastritis small (77% <1cm) polypoid multiple grade 1 confined to mucosa/submucosa (93%) slow-growing metastasis uncommon (5% LN) and not fatal
25 Management of type 1 ECL-cell tumours staging (EUS/CT) treat vitamin deficiencies, eradicate HP if present endoscopic polypectomy for raised lesions antrectomy and local excision for large (>1 cm) or numerous tumours gastrectomy only for tumours with clear-cut malignant features endoscopic follow-up ablation of new lesions surveillance for adenocarcinoma completion gastrectomy as last resort?? octreotide Gladdy RA et al. Ann Surg Oncol 2009; 16:
26 Type II ECL-cell tumours in Zollinger-Ellison syndrome hypertrophic oxyntic glands all patients have linear ECL-cell hyperplasia nodular ECL-cell hyperplasia and ECL-cell tumours are virtually confined to those who have underlying MEN-1 Solcia E et al. Am J Surg Pathol 1990; 14:
27 G cell tumour hypergastrinaemia corpus ECL-cell hyperplasia corpus ECL-cell dysplasia corpus ECL-cell neuro-endocrine tumours
28 Type II ECL-cell tumours in MEN 1 present in 13-30% of cases small (75% <1.5 cm) polypoid multiple grade 1 confined to mucosa/submucosa slow-growing metastasis unusual (30% LN) and rarely fatal
29 Management treat primary condition and investigate family eradicate HP if present endoscopic polypectomy for raised lesions local excision for large (>1 cm) or numerous tumours consider gastrectomy only for tumours with clear-cut malignant features endoscopic follow-up and ablation of new lesions completion gastrectomy as last resort?? octreotide
30 Type IV ECL-cell tumours spectacularly rare no gastritis no gastrinoma, ZE syndrome or MEN1 ECL -cell hyperplasia, dysplasia, multiple invasive tumours hypertrophic, distended oxyntic glands containing inspissated eosinophilic material hyperplastic vacuolated parietal cells ciliated metaplasia Ooi A et al (1995) Endocrine Pathol 3: 229 Abraham SC et al (2005) Am J Surg Pathol 29:969-75
31 Sporadic (type III) gastric NETs 13% of all gastric neuro-endocrine tumours males > females mainly corpus and of ECL-cell or X-cell type (antral G-cell or EC-cell tumours rare) no background ECL-cell hyperplasia usually solitary (but multiple polyps described) often have features of gastric carcinoma may produce a flushing syndrome (histamine) Rindi G et al. Gastroenterology 1993; 104:
32 Sporadic (type III) gastric NETs usually >2cm frequently deeply invasive carcinomas 76% muscularis propria 53% serosa frequently metastatic (LN 71%; distant 69%) significant mortality (27%) mean survival 28 months
33 Sporadic (type III) gastric NETs typically G2 tumours but some are G3 neuro-endocrine carcinomas usually large cell type vesicular nuclei, large nucleoli sometimes atypical mitoses may have a scirrhous pattern >10% Ki67 labelling index necrosis p53 expression Jiang S-X et al. Am J Surg Pathol 2006; 30:
34
35 Management small (<1cm), well differentiated G1 tumours, confined to submucosa without angioinvasion polypectomy confirm favourable histology and complete excision remainder gastrectomy
36 Gastric mixed tumours (MANECs) although gastric adenocarcinomas frequently contain neuro-endocrine cells, they rarely account for >30% AB/PAS) MANECs (by WHO criteria) are very uncommon endocrine component is usually grade 3 manage as conventional adenocarcinomas (similar prognosis) chromogranin
37 An important case 64 F. Polyp with superficial ulcer in stomach. not Gloucestershire slides!
38 64 F. Polyp with superficial ulcer in stomach.
39 64 F. Polyp with superficial ulcer in stomach. cytokeratin
40 64 F. Polyp with superficial ulcer in stomach. Here comes the total gastrectomy..
41 64 F. Polyp with superficial ulcer in stomach. Here comes the total gastrectomy.. synaptophysin
42 NET v carcinoma Four types of gastric chronic atrophic Zollinger-Ellison syndrome sporadic intrinsic abnormality of parietal cells The first is the commonest, is benign (unless..) and treated very conservatively (EMR/ER/surveillance)
43 Context in gastrointestinal NETs Rectum Stomach Stomach
44 Beware, though!
45 Differentiated duodenal neuro-endocrine tumours classical neuro-endocrine cell tumours: G cell, argyrophil, gastrin-containing EC cell, argentaffin, serotonin-containing A and B cell (glucagon and insulin) very rare tumours of unusual morphology: D cell, variably argyrophil, somatostatin-containing gangliocytic paraganglioma
46 Duodenal G-cell NET commonest duodenal neuro-endocrine tumours proximal duodenum usually small (<1cm) and G1, occasionally G2 trabecular pattern, may contain amyloid 1/3 functional (ZE syndrome) can be very small and difficult to detect
47
48 Duodenal G-cell NETs non-functional tumours usually benign behaving functional tumours have long natural history: lymph node metastases (often larger than primary) common if functional liver metastases late and rare prognosis with metastatic disease good with acid suppression or octreotide
49 Duodenal D-cell tumours 15-20% of duodenal neuro-endocrine tumours periampullary (haemorrhage, jaundice, pancreatitis) small intramural or polypoid tumours contain somatostatin always non-functional ~ 50% have type 1 neurofibromatosis <1% of NF-1 patients have duodenal tumours Garbrecht N et al. Endocr Relat Cancer 2008; 15:
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51 Is this pancreatic adenocarcinoma or metastatic prostatic carcinoma?
52 PAS PAS
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54
55 ? synaptophysin somatostatin
56 Duodenal D-cell NETs glandular architecture PAS-positive luminal cell borders psammoma bodies non-argentaffin non-argyrophil by Grimelius synaptophysin positive usually chromogranin A positive somatostatin positive
57 Duodenal D-cell NETs tumours of low grade malignancy lymph node metastasis in 25% (usually in larger tumours) distant metastasis very uncommon very good prognosis after local excision
58 Gangliocytic paraganglioma periampullary (haemorrhage, jaundice, pancreatitis) solitary intramural or polypoid tumours Up to 7cm any age always non-functional benign behaving (though rare LN mets) occasionally found in NF-1 patients triphasic histological components Hamid QA et al. Hum Pathol 1986;17:
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62 Gangliocytic paraganglioma spindle cells interweaving fascicles S-100 and neurofilament-positive
63 Gangliocytic paraganglioma spindle cells epithelioid cells nests and ribbons variably chromogranin + synaptophysin + usually contain PP, somatostatin may be psammoma bodies, amyloid synapto
64 Gangliocytic paraganglioma spindle cells epithelioid cells ganglion cells typical ganglion cells, with satellite cells, GFAP+ some merge with epithelioid cells zellballen-like arrangements
65 Duodenal neuro-endocrine carcinoma & MANEC rare large, bulky, ulcerating periampullary lesions sporadic small cell and large cell extensive necrosis metastases at presentation in 92% mean survival 8 months chromogranin A synaptophysin
66 Jejunal & ileal NETS EC-cell tumours contain serotonin and substance P classical argentaffin carcinoid pattern majority G1 (G3 neuro-endocrine carcinoma does not occur at this site) mutation and/or LOH of MEN1 gene (11q13) multiple in ~25% (worse outcome) multiple tumours are usually spread from a single tumour (X-chromosome inactivation analysis) sometimes EC-cell hyperplasia but not familial Guo et al, 2000
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70 Ileal neuro-endocrine tumours incidental finding obstruction/intussusception haemorrhage carcinoid syndrome when liver metastases or very bulky intraperitoneal disease intestinal ischaemia related to mesenteric sclerosis
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73 Behaviour of ileal NETs progression slow 5 year survival ~50% related to: metastases (liver, lymph node) size (>2 cm) angioinvasion G2 (Ki67 > 2%) unrelated to: depth of invasion multiplicity post-operative therapy partly governed by grade Dhall G et al. Hum Pathol 2012; 43:
74 Appendiceal neuro-endocrine tumours EC-cell tumours L-cell tumours goblet cell carcinoids and/or MANECs
75 Appendiceal neuro-endocrine tumours EC-cell tumours: 90% acinar, clear-cell, balloon-cell patterns grade 1 argentaffin, chromogranin A +ve contain serotonin and substance P may contain S-100-positive Schwann-like cells
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77 acinar balloon cell EC-cell tumours clear cell
78 Appendiceal neuro-endocrine tumours L-cell tumours: 5-10% trabecular or tubular grade 1 non-argentaffin but argyrophil often chromogranin A-negative contain enteroglucagons, PP or PYY may be misdiagnosed as goblet cell carcinoid or metastatic carcinoma (esp breast)
79 no intracytoplasmic mucin L-cell tumours
80 G1 appendiceal neuro-endocrine tumours metastasis uncommon but related to tumours >2 cm or with deep mesoappendiceal invasion BUT virtually all metastatic tumours present at original surgery right hemicolectomy is recommended when involvement of the resection margin deep (>3mm) mesoappendiceal invasion tumour size >2cm Plockinger U et al. Neuroendocrinology 2008; 87:
81 Goblet cell carcinoid females > males incidental or appendicitis often diffuse growth pattern may coexist with adenomas or conventional neuro-endocrine tumours propensity for transcoelomic spread, especially to ovary lymph node and liver metastases relatively unusual 11% have distant metastases at presentation 75% overall 5 year survival
82 Goblet cell carcinoid mixed tumour composed of: - mucous cells - enterocytes/colonocytes - endocrine cells (EC-cells or L-cells) - Paneth cells now regarded as MANEC by WHO and considered under adenocarcinoma of the appendix
83
84 synaptophysin
85 Clinical history 60M. Previous appendicitis and mass. Conservative treatment & subsequent appendicectomy.
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87
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89 Ki67/MIB1
90 Adenocarcinoma ex-goblet cell carcinoid
91 Tang classification for the natural history and prognosis of goblet cell carcinoids of the appendix
92 Goblet cell carcinoid / MANEC 20-30% have aggressive features nuclear pleomorphism >2/10 hpf mitoses solid sheets fused cribriform glands single file structures diffusely infiltrating signet ring cells conversely those on the benign end of the spectrum have a good prognosis, especially if small and confined to the appendix Tang LH et al. Am J Surg Pathol 2008; 32:
93
94 Management of goblet cell carcinoid/manec Right hemicolectomy with bilateral salpingo-oophorectomy except when, after extensive histological evaluation, tumour is < 10mm low grade (<2 mitoses/10 HPF) localised to appendiceal wall with no caecal, mesoappendiceal or serosal invasion Plockinger U et al. Neuroendocrinology 2008; 87:
95 Colorectal neuro-endocrine tumours grade 1-2 EC-cell tumours: usually in caecum and ascending colon argentaffin, contain serotonin and substance P grade 1-2 L-cell tumours: usually in rectum trabecular and argyrophil often chromogranin A negative but synaptophysin and SV2 positive contain enteroglucagons, glicentin, PP or PYY minor components of other peptides prostatic acid phosphatase (but not PSA) positive
96 Colorectal neuro-endocrine tumours proximal tumours larger than rectal tumours may arise in long-standing ulcerative colitis virtually never functioning apart from very rare carcinoid syndrome with EC cell tumours
97 synaptophysin
98
99 Colorectal neuro-endocrine tumours behaviour related to: size stage grade 78% metastatic tumours >2 cm 8% tumours <2 cm metastasised <3% tumours <1 cm metastasised 46% tumours invading muscularis propria metastasised
100 Management of colorectal neuro-endocrine tumours endoscopic resection for G1, T1a lesions small (<10mm) confined to mucosa/submucosa no lymphovascular invasion completely excised relatively common in the rectum remainder treated as for colorectal cancer
101 G3 colorectal neuro-endocrine carcinomas and MANECs bulky, rapidly growing masses large cell mostly in proximal colon and may be admixed with conventional adenocarcinoma small cell mostly in distal rectum/anal canal, sometimes admixed with squamous cell carcinoma virtually never functional usually positive for synaptophysin may arise in adenomas or in chronic UC median survival 5 months Gaffey MJ et al. Am J Surg Pathol 1990; 14:
102
103 The pathology of neuroendocrine tumours of the gut: take home messages site in the GI tract has a profound influence on the morphology, natural history, hormone elaboration, management & prognosis of NETs grade is an important factor in treatment and prognosis and is an important assessment. This is largely determined by proliferative activity and the Ki67/MIB1 score hyperplasia from chronic hyperstimulation and/or inherited abnormalities of neuro-endocrine cell growth are sometimes important in their pathogenesis important pathological determinants are site, cell type, degree of differentiation, stage and grade clinicopathological correlation is essential in determining management and discussion in an MDTM is beneficial a dataset for pathology reporting, developed through clinical and pathological consensus, is advised
104 Thank you for listening!
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