Small intestine cancer pathophysiology: Difference between revisions

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'''Small intestinal stromal tumors (GISTs):'''
'''Small intestinal stromal tumors (GISTs):'''
*These tumors are associated with older age and are rare before 40.<ref name="pmid25277795">{{cite journal |vauthors=Ma GL, Murphy JD, Martinez ME, Sicklick JK |title=Epidemiology of gastrointestinal stromal tumors in the era of histology codes: results of a population-based study |journal=Cancer Epidemiol. Biomarkers Prev. |volume=24 |issue=1 |pages=298–302 |date=January 2015 |pmid=25277795 |pmc=4294949 |doi=10.1158/1055-9965.EPI-14-1002 |url=}}</ref><ref name="pmid15648083">{{cite journal |vauthors=Nilsson B, Bümming P, Meis-Kindblom JM, Odén A, Dortok A, Gustavsson B, Sablinska K, Kindblom LG |title=Gastrointestinal stromal tumors: the incidence, prevalence, clinical course, and prognostication in the preimatinib mesylate era--a population-based study in western Sweden |journal=Cancer |volume=103 |issue=4 |pages=821–9 |date=February 2005 |pmid=15648083 |doi=10.1002/cncr.20862 |url=}}</ref><ref name="pmid15900576">{{cite journal |vauthors=Tryggvason G, Gíslason HG, Magnússon MK, Jónasson JG |title=Gastrointestinal stromal tumors in Iceland, 1990-2003: the icelandic GIST study, a population-based incidence and pathologic risk stratification study |journal=Int. J. Cancer |volume=117 |issue=2 |pages=289–93 |date=November 2005 |pmid=15900576 |doi=10.1002/ijc.21167 |url=}}</ref>
*They can be sporadic or inherited.


==Genetics==
==Genetics==

Revision as of 18:56, 13 January 2019

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Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1]; Associate Editor(s)-in-Chief: Qurrat-ul-ain Abid, M.D.[2], Parminder Dhingra, M.D. [3]

Overview

Adenocarcinoma is the most common sub-type of small intestine cancer. Second most common is carcinoid tumor. Adenocarcinomas can be polypoid, infiltrating or they appear as annular constricting lesions in small intestine. On gross pathology, napkin ring appearance or polypoidal fungatining mass are characteristic findings of small intestine cancer. Carcinoid tumors of the smalls intestine are mostly associated with malignant tumors of the other sites. Gastrointestinal stromal tumors (GISTs) are the most common benign tumors of the gastrointestinal (GI) tract. Small intestinal lymphomas are of low-grade histology and arise from mucosal-associated lymphoid tissues (MALT).

Pathophysiology

  • Pathophysiology of the small intestinal cancers is not much studied domain, as it is a rare condition.
  • Studies are being conducted to evaluate association with environmental risk factors.[1]
  • Pathophysiology of small intestinal cancers depend on the histological subtype.
  • Duodenal tumors are more common than the tumors of jejunum and illeum.[2]
  • Adenomas arise more proximally in the duodenum and lymphomas arise in jejunum and ileum.[3]
  • Low susceptibility of the small intestine to malignant changes can be explained by following:
    • Short exposure of the mucosa to carcinogens due to rapid transit of contents.
    • Liquid nature of the contents and less mucosal irritation.
    • Low bacterial load
    • High concentration of lymphoid tissue

Adenocarcinoma:

  • Adenocarcinoma are most common neoplasm of small bowel.
  • Their incidence is more in males.[4]
  • Adenocarcinoma of small intestine is more common in patients with colorectal cancer, suggesting their common pathophysiology.
  • Adenocarcinoma may develop from malignant changes in the polyps of small intestine.[5][6]
  • Long standing [Crohn's disease] is known as a risk factor of small intestine cancer.[7]
  • Certain hereditary conditions with intestinal polyps such as Adenomatous polyposis coli (ACP) predispose to adenocarcinoma of small intestine.
  • Adenocarcinoma are more common in duodenum.
  • Development of adenocarcinoma in duodenum may be explained by vigorous exposure of that part of intestine to different carcinogens, which gets diluted in the latter part of intestine.
  • Small Intestinal neuroendocrine tumors (SI-NETs) are the most common gastrointestinal neuroendocrine tumors.[8]
  • The oncofetal protein IMP3 is a marker that plays a role in the growth of neuroendocrine cells.[9]

Non-Hodgkin Lymphoma:

  • Small intestinal lymphomas are of low-grade histology and arise from mucosal-associated lymphoid tissues (MALT) present in ileum and jejunum.
  • Sometimes distinct clinicopathologic entities arise from these mucosal-associated lymphoid tissues (MALT), such as immunoproliferative small intestinal disease, primary intestinal T-cell lymphoma and multiple lymphomatous polyposis.[10]
  • Lymphoma may present as primary tumor of small intestine or may be part of systemic disease.
  • After stomach, small intestine is the most common extra-nodal site of presentation of non-Hodgkin lymphomas and it represents 4% to 20% of all the non-Hodgkin lymphomas.
  • The diagnosis of small intestinal lymphoma can be made using following criteria:[11][12]
    • Absence of peripheral or mediastinal lymphadenopathy
    • White blood cell count should be normal
    • Predominant involvement of GI tract
    • Liver or spleen should not be involved

Small intestinal stromal tumors (GISTs):

  • GISTs are the most benign tumors of GIT and rarely can be malignant.
  • They typically develop in older age.
  • Stromal tumors are most common in the stomach, 60–70% of the stromal tumors, followed by small intestine which makes 20–25% of all the stromal tumors of GI tract, colon and rectum makes 5% and esophagus is less than 5%.
  • One of the subset of intestinal stromal cell tumors is the GI autonomic nerve tumors (GANTs). Stromal tumors can be differentiated from other tumors of small intestine by their cell specific markers.
  • GISTs express following stromal cell markers:[13]
    • 70% of GISTs are positive for CD34
    • 20–30% are positive for smooth muscle actin (SMA)
    • 10% are positive for S100 protein
    • <5% are positive for desmin

Associations

Some GIT disorders such as inflammatory diseases of GIT may predispose to malignancy. Some of the associations are:[14]


Adenocarcinoma:

  • Adenocarcinoma of the smalls intestine originate locally or can be associated with malignant tumors of other sites.
  • Rarely it can develop fom malignant changes in polyps present in the small intestine.
  • Dietary factors, tobacco, and obesity can also play a role.[15][16][17][18][19]

Carcinoid Tumors:

  • Carcinoid tumors of small intestine are associated with Multiple Endocrine Neoplasia type I (MEN-I). [20][21]


Non-Hodgkin Lymphoma:

  • Some of the association of non-Hodgkin lymphomas are :[10]
    • Helicobacter pylori infection[22]
    • Immunosuppression after solid-organ transplantation
    • Celiac disease[23]
    • Inflammatory bowel disease
    • Human immunodeficiency virus (HIV)[24]
    • Organ transplant[25]


Small intestinal stromal tumors (GISTs):

  • These tumors are associated with older age and are rare before 40.[26][27][28]
  • They can be sporadic or inherited.

Genetics

Cancer of small intestine can arise sporadically or they are associated with genetic diseases.

Adenocarcinoma:

  • Small intestine adenocarcinomas arise from adenomas.
  • Adenoma-carcinoma sequence is thought to play the role in development of small intestine adenocarcinoma but is not understood by the researchers yet.[29]
  • Adenocarcinoma is thought to be associated with some genetic diseases such as:
  • Herditary Non-Polyposis colosis(HNPCC)[30][4]
  • Gardner's syndrome[31]
  • Peutz-Jeghers syndrome[6]
  • Familial Adenosis Polyposis (FAP)[32]

Carcinoid Tumors:

  • Carcinoid tumor of small intestine are part of manifestation of a genetic disorder MEN type1.

Non-Hodgkin Lymphoma:

  • Lymphomas of small intestine have no established genetic predisposition.

Small intestinal stromal tumors (GISTs):

  • Stromal tumors of small intestine may be associated with activating mutations in the KIT or platelet-derived growth factor receptor alpha (PDGFRA) genes.[33][34]

Gross Pathology

Adenocarcinoma:

  • Adenocarcinomas can be polypoid, infiltrating, or as annular constricting lesions is small intestine.
  • Polyps and adenomas of small intestine are considered precursor lesions of adenocarcinoma.[35]
Adenocarcinoma of the small intestine. Endoscopic image of adenocarcinoma of duodenum. Source: Wikimedia commons



Carcinoid Tumors:

  • They are diverse neoplasms emerging from the endocrine cells of the intestinal mucosa.[9]
Carcinoid tumor of small intestine invading plica circularisSource: Wikimedia commons
Multiple Carcinoid tumor of the small intestine Source: Wikimedia commons


Non-Hodgkin Lymphoma:

  • Lymphomas of small intestine present with suspicious growths in submucosa with normal appearing muscosa.
  • Endoscopic evaluation may show multifocal involvement and large biopsies are required for diagnoses.


Small intestinal stromal tumors (GISTs):

  • Instestinal stromal cell tumors should be differentiated from leiomyosarcomas and leiomyomas. They differ clinically and pathogenetically from leiomyosarcomas and leiomyomas. Leimyomas occur in the GI tract, commonly in the esophagus.
Gastrointestinal stromal tumor in the jejunum, endoscopic image.Wikimedia commons

Microscopic Pathology

Adenocarcinoma:

  • Primary adenocarcinoma consists of 40% of cases of malignant tumors of small intestine and it is the most common histologic type. [36][37][38]
  • Adenocarcinoma of the small bowel present as cluster of malignant cells distorting the normal structure of wall of small intestine.


Carcinoid Tumors:

  • These tumors originate from enterochromaffin (EC) cells and secrete serotonin.[39]
  • Carcinoid tumors are positive for synaptophysin or chromogranin, which can be demonstrated by immunohistochemical staining.[37]
Typical histological appearance of neuroendocrine carcinoma, showing neuroednocrine tumor cells(bottom), Paneth cells(red cells at the base of the crypt) and intestinal villi.Source: Wikimedia Commons



Non-Hodgkin Lymphoma:

  • Histologically,cnon-Hodgkin lymphomas may be low grade or high grade tumor of small intestine.
  • They may be of B-cell or T-cell origin.[40][41]
  • Their cell lineage can be identified using immunohistochemical staining.[42]
  • Gastric lymphomas are divided into two histologic subtypes:
    • Extranodal marginal zone B cell lymphoma of mucosa (MALT)
    • Diffuse large B cell lymphoma


Small intestinal stromal tumors (GISTs):

  • Histologically, GISTs may resemble leiomyosarcomas so,should be differentiated from them.
  • The microscopic appearance of gastrointestinal stromal tumors (GISTs) resembles spindle cell or epithelioid.
    • Spindle cell type are eosinophilic cells arranged in the form of whorls or fascicles.[43]
    • Epithelioid GISTs are rounded cells with oval nuclei and vesicular chromatin and appears nested[44]
  • On immunohistochemical staining they are positive for molecular markers CD117 antigen.

References

  1. ↑ Severson RK, Schenk M, Gurney JG, Weiss LK, Demers RY (February 1996). "Increasing incidence of adenocarcinomas and carcinoid tumors of the small intestine in adults". Cancer Epidemiol. Biomarkers Prev. 5 (2): 81–4. PMID 8850266.
  2. ↑ Dabaja BS, Suki D, Pro B, Bonnen M, Ajani J (August 2004). "Adenocarcinoma of the small bowel: presentation, prognostic factors, and outcome of 217 patients". Cancer. 101 (3): 518–26. doi:10.1002/cncr.20404. PMID 15274064.
  3. ↑ Chow JS, Chen CC, Ahsan H, Neugut AI (August 1996). "A population-based study of the incidence of malignant small bowel tumours: SEER, 1973-1990". Int J Epidemiol. 25 (4): 722–8. PMID 8921448.
  4. ↑ 4.0 4.1 Rodriguez-Bigas MA, Vasen HF, Lynch HT, Watson P, Myrhøj T, Järvinen HJ, Mecklin JP, Macrae F, St John DJ, Bertario L, Fidalgo P, Madlensky L, Rozen P (July 1998). "Characteristics of small bowel carcinoma in hereditary nonpolyposis colorectal carcinoma. International Collaborative Group on HNPCC". Cancer. 83 (2): 240–4. PMID 9669805.
  5. ↑ Lynch HT, Smyrk TC, Lynch PM, Lanspa SJ, Boman BM, Ens J, Lynch JF, Strayhorn P, Carmody T, Cristofaro G (November 1989). "Adenocarcinoma of the small bowel in lynch syndrome II". Cancer. 64 (10): 2178–83. PMID 2804907.
  6. ↑ 6.0 6.1 Giardiello FM, Brensinger JD, Tersmette AC, Goodman SN, Petersen GM, Booker SV, Cruz-Correa M, Offerhaus JA (December 2000). "Very high risk of cancer in familial Peutz-Jeghers syndrome". Gastroenterology. 119 (6): 1447–53. PMID 11113065.
  7. ↑ Palascak-Juif V, Bouvier AM, Cosnes J, Flourié B, Bouché O, Cadiot G, Lémann M, Bonaz B, Denet C, Marteau P, Gambiez L, Beaugerie L, Faivre J, Carbonnel F (September 2005). "Small bowel adenocarcinoma in patients with Crohn's disease compared with small bowel adenocarcinoma de novo". Inflamm. Bowel Dis. 11 (9): 828–32. PMID 16116317.
  8. ↑ Modlin, Irvin M.; Champaneria, Manish C.; Chan, Anthony K.C.; Kidd, Mark (2007). "A Three-Decade Analysis of 3,911 Small Intestinal Neuroendocrine Tumors: The Rapid Pace of No Progress". The American Journal of Gastroenterology. 102 (7): 1464–1473. doi:10.1111/j.1572-0241.2007.01185.x. ISSN 0002-9270.
  9. ↑ 9.0 9.1 Massironi S, Del Gobbo A, Cavalcoli F, Fiori S, Conte D, Pellegrinelli A, Milione M, Ferrero S (November 2017). "IMP3 expression in small-intestine neuroendocrine neoplasms: a new predictor of recurrence". Endocrine. 58 (2): 360–367. doi:10.1007/s12020-017-1249-x. PMID 28210937.
  10. ↑ 10.0 10.1 Crump M, Gospodarowicz M, Shepherd FA (June 1999). "Lymphoma of the gastrointestinal tract". Semin. Oncol. 26 (3): 324–37. PMID 10375089.
  11. ↑ Cooper MJ, Williamson RC (December 1985). "Enteric adenoma and adenocarcinoma". World J Surg. 9 (6): 914–20. PMID 4082613.
  12. ↑ Sweetenham JW, Mead GM, Wright DH, McKendrick JJ, Jones DH, Williams CJ, Whitehouse JM (September 1989). "Involvement of the ileocaecal region by non-Hodgkin's lymphoma in adults: clinical features and results of treatment". Br. J. Cancer. 60 (3): 366–9. PMC 2247183. PMID 2789943.
  13. ↑ Schlotzhauer WS, Chortyk OT, Austin PR (1976). "Pyrolysis of chitin, a potential tobacco extender". J Agric Food Chem. 24 (1): 177–80. PMID 1432-2307 Check |pmid= value (help).
  14. ↑ Gill SS, Heuman DM, Mihas AA (October 2001). "Small intestinal neoplasms". J. Clin. Gastroenterol. 33 (4): 267–82. PMID 11588539.
  15. ↑ Chow WH, Linet MS, McLaughlin JK, Hsing AW, Chien HT, Blot WJ (March 1993). "Risk factors for small intestine cancer". Cancer Causes Control. 4 (2): 163–9. PMID 8481495.
  16. ↑ Neugut AI, Jacobson JS, Suh S, Mukherjee R, Arber N (March 1998). "The epidemiology of cancer of the small bowel". Cancer Epidemiol. Biomarkers Prev. 7 (3): 243–51. PMID 9521441.
  17. ↑ Wu AH, Yu MC, Mack TM (March 1997). "Smoking, alcohol use, dietary factors and risk of small intestinal adenocarcinoma". Int. J. Cancer. 70 (5): 512–7. PMID 9052748.
  18. ↑ Solem CA, Harmsen WS, Zinsmeister AR, Loftus EV (January 2004). "Small intestinal adenocarcinoma in Crohn's disease: a case-control study". Inflamm. Bowel Dis. 10 (1): 32–5. PMID 15058524.
  19. ↑ Jess T, Winther KV, Munkholm P, Langholz E, Binder V (February 2004). "Intestinal and extra-intestinal cancer in Crohn's disease: follow-up of a population-based cohort in Copenhagen County, Denmark". Aliment. Pharmacol. Ther. 19 (3): 287–93. PMID 14984375.
  20. ↑ Heymann MF, Hamy A, Triau S, Miraillé E, Toquet C, Chomarat H, Cohen C, Maitre F, Le Bodie MF (2004). "Endocrine tumors of the duodenum. A study of 55 cases relative to clinicopathological features and hormone content". Hepatogastroenterology. 51 (59): 1367–71. PMID 15362754.
  21. ↑ Leoncini E, Carioli G, La Vecchia C, Boccia S, Rindi G (January 2016). "Risk factors for neuroendocrine neoplasms: a systematic review and meta-analysis". Ann. Oncol. 27 (1): 68–81. doi:10.1093/annonc/mdv505. PMID 26487581.
  22. ↑ Aull MJ, Buell JF, Peddi VR, Trofe J, Beebe TM, Hanaway MJ, Roy-Chaudhury P, Alloway RR, First MR, Woodle ES (January 2003). "MALToma: a Helicobacter pylori-associated malignancy in transplant patients: a report from the Israel Penn International Transplant Tumor Registry with a review of published literature". Transplantation. 75 (2): 225–8. doi:10.1097/01.TP.0000040875.50963.2C. PMID 12548128.
  23. ↑ Catassi C, Fabiani E, Corrao G, Barbato M, De Renzo A, Carella AM, Gabrielli A, Leoni P, Carroccio A, Baldassarre M, Bertolani P, Caramaschi P, Sozzi M, Guariso G, Volta U, Corazza GR (March 2002). "Risk of non-Hodgkin lymphoma in celiac disease". JAMA. 287 (11): 1413–9. PMID 11903028.
  24. ↑ Coté TR, Biggar RJ, Rosenberg PS, Devesa SS, Percy C, Yellin FJ, Lemp G, Hardy C, Geodert JJ, Blattner WA (November 1997). "Non-Hodgkin's lymphoma among people with AIDS: incidence, presentation and public health burden. AIDS/Cancer Study Group". Int. J. Cancer. 73 (5): 645–50. PMID 9398040.
  25. ↑ McTamaney JP, Neifeld JP, Mendez-Picon G, Lee HM (1981). "Primary gastric lymphoma following renal transplantation". J Surg Oncol. 18 (3): 265–8. PMID 7031373.
  26. ↑ Ma GL, Murphy JD, Martinez ME, Sicklick JK (January 2015). "Epidemiology of gastrointestinal stromal tumors in the era of histology codes: results of a population-based study". Cancer Epidemiol. Biomarkers Prev. 24 (1): 298–302. doi:10.1158/1055-9965.EPI-14-1002. PMC 4294949. PMID 25277795.
  27. ↑ Nilsson B, Bümming P, Meis-Kindblom JM, Odén A, Dortok A, Gustavsson B, Sablinska K, Kindblom LG (February 2005). "Gastrointestinal stromal tumors: the incidence, prevalence, clinical course, and prognostication in the preimatinib mesylate era--a population-based study in western Sweden". Cancer. 103 (4): 821–9. doi:10.1002/cncr.20862. PMID 15648083.
  28. ↑ Tryggvason G, Gíslason HG, Magnússon MK, Jónasson JG (November 2005). "Gastrointestinal stromal tumors in Iceland, 1990-2003: the icelandic GIST study, a population-based incidence and pathologic risk stratification study". Int. J. Cancer. 117 (2): 289–93. doi:10.1002/ijc.21167. PMID 15900576.
  29. ↑ Wheeler JM, Warren BF, Mortensen NJ, Kim HC, Biddolph SC, Elia G, Beck NE, Williams GT, Shepherd NA, Bateman AC, Bodmer WF (February 2002). "An insight into the genetic pathway of adenocarcinoma of the small intestine". Gut. 50 (2): 218–23. PMC 1773117. PMID 11788563.
  30. ↑ Zhang MQ, Chen ZM, Wang HL (April 2006). "Immunohistochemical investigation of tumorigenic pathways in small intestinal adenocarcinoma: a comparison with colorectal adenocarcinoma". Mod. Pathol. 19 (4): 573–80. doi:10.1038/modpathol.3800566. PMID 16501564.
  31. ↑ Kawashima A, Goldman SM, Fishman EK, Kuhlman JE, Onitsuka H, Fukuya T, Masuda K (February 1994). "CT of intraabdominal desmoid tumors: is the tumor different in patients with Gardner's disease?". AJR Am J Roentgenol. 162 (2): 339–42. doi:10.2214/ajr.162.2.8310922. PMID 8310922.
  32. ↑ Abrahams NA, Halverson A, Fazio VW, Rybicki LA, Goldblum JR (November 2002). "Adenocarcinoma of the small bowel: a study of 37 cases with emphasis on histologic prognostic factors". Dis. Colon Rectum. 45 (11): 1496–502. doi:10.1097/01.DCR.0000034134.49346.5E. PMID 12432298.
  33. ↑ Rubin BP, Fletcher JA, Fletcher CD (January 2000). "Molecular Insights into the Histogenesis and Pathogenesis of Gastrointestinal Stromal Tumors". Int. J. Surg. Pathol. 8 (1): 5–10. doi:10.1177/106689690000800105. PMID 11493959.
  34. ↑ Miettinen M, Lasota J (January 2001). "Gastrointestinal stromal tumors--definition, clinical, histological, immunohistochemical, and molecular genetic features and differential diagnosis". Virchows Arch. 438 (1): 1–12. PMID 11213830.
  35. ↑ Levine JS, Ahnen DJ (December 2006). "Clinical practice. Adenomatous polyps of the colon". N. Engl. J. Med. 355 (24): 2551–7. doi:10.1056/NEJMcp063038. PMID 17167138.
  36. ↑ Barclay TH, Schapira DV (March 1983). "Malignant tumors of the small intestine". Cancer. 51 (5): 878–81. PMID 6821853.
  37. ↑ 37.0 37.1 Lee MJ, Lee HS, Kim WH, Choi Y, Yang M (May 2003). "Expression of mucins and cytokeratins in primary carcinomas of the digestive system". Mod. Pathol. 16 (5): 403–10. doi:10.1097/01.MP.0000067683.84284.66. PMID 12748245.
  38. ↑ Chen ZM, Wang HL (October 2004). "Alteration of cytokeratin 7 and cytokeratin 20 expression profile is uniquely associated with tumorigenesis of primary adenocarcinoma of the small intestine". Am. J. Surg. Pathol. 28 (10): 1352–9. PMID 15371952.
  39. ↑ Sei Y, Feng J, Zhao X, Forbes J, Tang D, Nagashima K, Hanson J, Quezado MM, Hughes MS, Wank SA (July 2016). "Polyclonal Crypt Genesis and Development of Familial Small Intestinal Neuroendocrine Tumors". Gastroenterology. 151 (1): 140–51. doi:10.1053/j.gastro.2016.03.007. PMC 5578471. PMID 27003604.
  40. ↑ Harris NL, Jaffe ES, Stein H, Banks PM, Chan JK, Cleary ML, Delsol G, De Wolf-Peeters C, Falini B, Gatter KC (September 1994). "A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group". Blood. 84 (5): 1361–92. PMID 8068936.
  41. ↑ Harris NL, Jaffe ES, Diebold J, Flandrin G, Muller-Hermelink HK, Vardiman J, Lister TA, Bloomfield CD (December 1999). "World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: report of the Clinical Advisory Committee meeting-Airlie House, Virginia, November 1997". J. Clin. Oncol. 17 (12): 3835–49. doi:10.1200/JCO.1999.17.12.3835. PMID 10577857.
  42. ↑ Lewin KJ, Ranchod M, Dorfman RF (August 1978). "Lymphomas of the gastrointestinal tract: a study of 117 cases presenting with gastrointestinal disease". Cancer. 42 (2): 693–707. PMID 354774.
  43. ↑ Fletcher CD, Berman JJ, Corless C, Gorstein F, Lasota J, Longley BJ, Miettinen M, O'Leary TJ, Remotti H, Rubin BP, Shmookler B, Sobin LH, Weiss SW (April 2002). "Diagnosis of gastrointestinal stromal tumors: a consensus approach". Int. J. Surg. Pathol. 10 (2): 81–9. doi:10.1177/106689690201000201. PMID 12075401.
  44. ↑ Medeiros F, Corless CL, Duensing A, Hornick JL, Oliveira AM, Heinrich MC, Fletcher JA, Fletcher CD (July 2004). "KIT-negative gastrointestinal stromal tumors: proof of concept and therapeutic implications". Am. J. Surg. Pathol. 28 (7): 889–94. PMID 15223958.

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