International Journal of Colorectal Disease

, Volume 22, Issue 10, pp 1239–1248 | Cite as

Malignant neoplasms of the appendix

  • Mark E. O’Donnell
  • Stephen A. Badger
  • Garth C. Beattie
  • Jim Carson
  • W. Ian H. Garstin
Original Article

Abstract

Background

Appendiceal neoplasms, first described in 1882, are still rare, with pre-operative diagnosis invariably difficult. We present our 10-year experience of these lesions with a review of current epidemiology, pathology and treatment modalities.

Materials and methods

A retrospective histopathological review of all appendicectomy specimens was completed between April 1994 and December 2003 to identify patients diagnosed with malignant neoplasms. Patient demographics, operative details, histopathology and clinical outcomes were obtained from case notes. A literature search of the PubMed database was then performed using the medical search headings; appendix, tumour, neoplasm and malignancy.

Results

Twenty-two patients (eight men) were identified during the study period, with no age difference between gender (mean age in women 58, range 14–83 vs mean age in men 55, range 16–78). Eleven patients were found to have carcinoid-type tumours, eight patients with adenocarcinomas and three patients with lymphomas. Other appendiceal pathologies were identified after appendicectomies, hemicolectomy and oophorectomy. Mean follow-up was 41 months (range 1–125 months). Fourteen patients were alive at the end of follow-up. Patients with classical carcinoid tumours (CCT) had better outcomes than patients with the goblet cell carcinoid, adenocarcinoma and lymphoma.

Conclusions

From our own experience and a subsequent review of the literature, we recommend right hemicolectomy as the treatment of choice for all malignant appendiceal neoplasms, except for small CCT less than 2 cm in diameter at the tip of the appendix, with a low proliferative index, without angiolymphatic or mesoappendiceal extension. Further adjuvant therapy should be considered after oncological assessment.

Keywords

Appendix Carcinoid Goblet cell Adenocarcinoma Lymphoma 

References

  1. 1.
    Adiss DG, Shaffer N, Fowler BS, Tauxe RV (1990) The epidemiology of appendicitis and appendectomy in the United States. Am J Epidemiol 132:910–925Google Scholar
  2. 2.
    Berger A (1882) Ein Fall von Krebs des Wurmfortsatzes. Ber Klin Wochenschr 19:610Google Scholar
  3. 3.
    Collins DC (1963) 71,000 human appendix specimens: a final report summarizing forty years’ study. Am J Proctol 14:365–381Google Scholar
  4. 4.
    Connor SJ, Hanna GB, Frizelle FA (1998) Appendiceal tumors: retrospective clinicopathologic analysis of appendiceal tumors from 7,970 appendectomies. Dis Colon Rectum 41:75–80PubMedCrossRefGoogle Scholar
  5. 5.
    O’Donnell ME, Carson J, Garstin WIH (2007) Surgical treatment of malignant carcinoid tumours of the appendix. Int J Clin Pract 61(3):431–437PubMedCrossRefGoogle Scholar
  6. 6.
    McGory ML, Maggard MA, Kang H, O’Connell JB, Ko CY (2005) Malignancies of the appendix: beyond case series reports. Dis Colon Rectum 48:2264–2271PubMedCrossRefGoogle Scholar
  7. 7.
    Butler JA, Houshair A, Lin F, Wilson SE (1994) Goblet cell carcinoid of the appendix. Am J Surg 168:685–687PubMedCrossRefGoogle Scholar
  8. 8.
    Cortina R, McCormick J, Kolm P, Perry RR (1995) Management and prognosis of adenocarcinoma of the appendix. Dis Colon Rectum 38:848–852PubMedCrossRefGoogle Scholar
  9. 9.
    Deans GT, Spence RAJ (1995) Neoplastic lesions of the appendix. Br J Surg 82:229–306CrossRefGoogle Scholar
  10. 10.
    Nitecki SS, Wolff BG, Schlinkert R, Sarr MG (1994) The natural history of surgically treated primary adenocarcinoma of the appendix. Ann Surg 219:51–57PubMedCrossRefGoogle Scholar
  11. 11.
    Lyss AP (1988) Appendiceal malignancies. Semin Oncol 15:129–137PubMedGoogle Scholar
  12. 12.
    Sandor A, Modulin IM (1998) A retrospective analysis of 1570 appendiceal carcinoids. Am J Gastroenterol 93:422–428PubMedCrossRefGoogle Scholar
  13. 13.
    Rutledge RH, Alexander JW (1992) Primary appendiceal malignancies. Surgery 111:244–250PubMedGoogle Scholar
  14. 14.
    Hananel N, Powsner E, Wolloch Y (1998) Adenocarcinoma of the appendix: an unusual case. Eur J Surg 164:859–862PubMedCrossRefGoogle Scholar
  15. 15.
    Arnold R, McCallion K, McGailie C (2006) Goblet cell carcinoids of the appendix. Ulster Med J 75: 40–45PubMedGoogle Scholar
  16. 16.
    McCusker ME, Cote TR, Clegg LX, Sobin LH (2002) Primary malignant neoplasms of the appendix: a population-based study from the surveillance, epidemiology and end-results program, 1973–1998. Cancer 94:3307–3312PubMedCrossRefGoogle Scholar
  17. 17.
    Hemminki K, Li X (2001) Incidence trends and risk factors of carcinoid tumors: a nationwide epidemiological study from Sweden. Cancer 92:2204–2210PubMedCrossRefGoogle Scholar
  18. 18.
    Godwin JD II (1975) Carcinoid tumors. An analysis of 2837 cases. Cancer 36:560–569PubMedCrossRefGoogle Scholar
  19. 19.
    Anderson JR, Wilson BG (1985) Carcinoid tumours of the appendix. Br J Surg 72:545–546PubMedCrossRefGoogle Scholar
  20. 20.
    Moertel CL, Weiland LH, Telander RL (1990) Carcinoid tumor of the appendix in the first two decades of life. J Pediatr Surg 25:1073–1075PubMedCrossRefGoogle Scholar
  21. 21.
    Modlin IM, Lye KD, Kidd M (2003) A 5-decade analysis of 13 715 carcinoid tumours. Cancer 97:934–959PubMedCrossRefGoogle Scholar
  22. 22.
    Roggo A, Wood WC, Ottinger LW (1993) Carcinoid tumours of the appendix. Ann Surg 217:385–390PubMedCrossRefGoogle Scholar
  23. 23.
    Hermans JJ, Hermans AL, Risseeuw GA, Verhaar JC, Meradji M (1993) Appendicitis caused by carcinoid tumour. Radiology 188:71–72PubMedGoogle Scholar
  24. 24.
    Nwiloh JO, Pillarisetty S, Moscovic EA, Freeman HP (1990) Carcinoid tumours. J Surg Oncol 45(4):261–264PubMedCrossRefGoogle Scholar
  25. 25.
    Markgraf WH, Dunn TM (1964) Appendiceal carcinoid with carcinoid syndrome. Am J Surg 107:730–732PubMedCrossRefGoogle Scholar
  26. 26.
    Johnston WH, Waisman J (1971) Carcinoid tumour of the vermiform appendix with Cushing’s syndrome. Cancer 27:681–686PubMedCrossRefGoogle Scholar
  27. 27.
    Kema IP, de Vries EG, Schellings AM, Postmus PE, Muskiet FA (1992) Improved diagnosis of carcinoid tumours by measurement of platelet serotonin. Clin Chem 38:534–540PubMedGoogle Scholar
  28. 28.
    King CM, Reznek RH, Bomanji J, Ur E, Britton KE, Grossman AB, Besser GM (1993) Imaging neuroendocrine tumours with radiolabelled somatostatin analogues and X-ray computed tomography: a comparative study. Clin Radiol 48:386–391PubMedCrossRefGoogle Scholar
  29. 29.
    Stivanello M, Berruti A, Torta M, Termine A, Tampellini M, Gorzegno G, Angeli A, Dogliotti L (2001) Circulating chromogranin A in the assessment of patients with neuroendocrine tumours. A single institutional experience. Ann Oncol 12 (Suppl 2):S73–S77PubMedCrossRefGoogle Scholar
  30. 30.
    Janson ET, Holmberg L, Stridsberg M, Eriksson B, Theodorsson E, Wilander E, Oberg K (1997) Carcinoid tumors: analysis of prognostic factors and survival in 301 patients from a tertiary referral centre. Ann Oncol 8:685–690PubMedCrossRefGoogle Scholar
  31. 31.
    Williams ED, Sandler M (1963) The classification of carcinoid tumours. Lancet 1:238–239PubMedCrossRefGoogle Scholar
  32. 32.
    Soga J, Tazawa K (1971) Pathologic analysis of carcinoids. Histologic re-evaluation of 62 cases. Cancer 28:990–998PubMedCrossRefGoogle Scholar
  33. 33.
    Capella C, Heitz PU, Hofler H, Solcia E, Kloppel G (1995) Revised classification of neuroendocrine tumours of the lung, pancreas and gut. Virchows Arch 425:547–560PubMedCrossRefGoogle Scholar
  34. 34.
    Van Eeden S, Quaedvlieg PF, Taal BG, Offerhaus GJ, Lamers CB, Van Velthuysen ML (2002) Classification of low-grade neuroendocrine tumours of the midgut and unknown origin. Hum Pathol 33:1126–1132PubMedCrossRefGoogle Scholar
  35. 35.
    Syracuse DC, Perzin KH, Price JB, Wiedel PD, Mesa-Tejada R (1979) Carcinoid tumours of the appendix. Mesoappendiceal extension and nodal metastases. Ann Surg 190:58–63PubMedCrossRefGoogle Scholar
  36. 36.
    Moertel CG, Weiland LH, Nagorney DM, Dockerty MB (1987) Carcinoid tumour of the appendix: treatment and prognosis. N Engl J Med 317:1699–1701PubMedCrossRefGoogle Scholar
  37. 37.
    Goede AC, Caplin ME, Winslet MC (2003) Carcinoid tumour of the appendix. Br J Surg 90:1317–1322PubMedCrossRefGoogle Scholar
  38. 38.
    Jonsson T, Johannsson JH, Hallgrimsson JG (1989) Carcinoid tumours of the appendix in children younger than 16 years. A retrospective clinical and pathologic study. Acta Chir Scand 155:113–116PubMedGoogle Scholar
  39. 39.
    Dhillon AP, Williams RA, Rode J (1992) Age, site and distribution of subepithelial neurosecretory cells in the appendix. Pathology 24:56–59PubMedGoogle Scholar
  40. 40.
    Ridolfi R, Amaducci L, Derni S, Fabbri L, Innocenti MP, Vignuteilli P (1991) Chemotherapy with 5-fluoracil and streptozotocin in carcinoid tumours of gastrointestinal origin: experiences with 13 patients. J Chemother 3:328–331PubMedGoogle Scholar
  41. 41.
    Arnold R, Neuhaus C, Benning R, Schwerk WB, Trautmann ME, Joseph K, Bruns C (1993) Somatostatin analog Sandostatin and inhibition of tumor growth in patients with metastatic endocrine gastroenteropancreatic tumors. World J Surg 72:511–519CrossRefGoogle Scholar
  42. 42.
    Buchanan KD (1993) Effects of Sandostatin on neuroendocrine tumours of the gastrointestinal system. Recent Results Cancer Res 129:45–55PubMedGoogle Scholar
  43. 43.
    Debas HT, Gittes G (1993) Somatostatin analogue therapy in functioning neuroendocrine gut tumors. Digestion 54(Suppl 1):68–71PubMedCrossRefGoogle Scholar
  44. 44.
    Saltz L, Trochanowski B, Buckley M, Heffernan B, Niedzwiecki D, Tao Y, Kelsen D (1993) Octreotide as an antineoplastic agent in the treatment of functional and nonfunctional neuroendocrine tumors. Cancer 72:244–248PubMedCrossRefGoogle Scholar
  45. 45.
    Janson ET, Oberg K (1993) Long-term management of the carcinoid syndrome. Treatment with octreotide alone and in combination with α-interferon. Acta Oncol 72:244–248Google Scholar
  46. 46.
    Moertel CG, Johnson CM, McKusick MA, Martin JK Jr, Nagorney DM, Kvols LK, Rubin J, Kunselman S (1994) The management of patients with advanced carcinoid tumors and islet cell carcinomas. Ann Intern Med 120:302–309PubMedGoogle Scholar
  47. 47.
    Gagne F, Fortin P, Dufour V, Delage C (1969) Tumeurs de l’appendice associant des carretteres histologiques de cardinoide et d’adenocarcinome. Ann Anat Pathol 14:393–406Google Scholar
  48. 48.
    Berardi RS, Lee SS, Chen HP (1988) Goblet cell carcinoids of the appendix. Surg Gynecol Obstet 167:81–86PubMedGoogle Scholar
  49. 49.
    Anderson NH, Somerville JE, Johnston CF, Hayes DM, Buchanan KD, Sloan JM (1991) Appendiceal goblet cell carcinoids: a clinicopathological and immunohistochemical study. Histopathology 18:61–65PubMedCrossRefGoogle Scholar
  50. 50.
    Kanthan R, Saxena A, Kanthan SC (2001) Goblet cell carcinoids of the appendix: immunophenotype and ultrastructural study. Arch Pathol Lab Med 125:386–390PubMedGoogle Scholar
  51. 51.
    Edmonds P, Merino MJ, LiVolsi VA, Duray PH (1984) Adenocarcinoid (mucinous carcinoid) of the appendix. Gastroenterology 86:302–309PubMedGoogle Scholar
  52. 52.
    Ramnani DM, Wistuba II, Behrens C, Gazdar AF, Sobin LH, Albores-Saavedra J (1999) K-ras and p53 mutations in the pathogenesis of classical and goblet cell carcinoids of the appendix. Cancer 86:14–21PubMedCrossRefGoogle Scholar
  53. 53.
    Chen KTK (1990) Appendiceal adenocarcinoid with ovarian metastases. Gynecol Oncol 38:268–286CrossRefGoogle Scholar
  54. 54.
    Warkel RL, Cooper PH, Helwig EB (1978) Adenocarcinoid, a mucin-producing tumour of the appendix. Cancer 42:2781–2793PubMedCrossRefGoogle Scholar
  55. 55.
    Klein E, Rosen M (1996) Bilateral Krukenberg tumours due to appendiceal mucinous carcinoid. Int J Gynecol Pathol 15:85–88PubMedCrossRefGoogle Scholar
  56. 56.
    Collins DC (1955) A study of 50,000 specimens of the human vermiform appendix. Surg Gynecol Obstet 101:437–445PubMedGoogle Scholar
  57. 57.
    Gilhome RW, Johnston DH, Clark J, Kyld J (1984) Primary adenocarcinoma of the vermiform appendix: report of a series of ten cases and review of the literature. Br J Surg 71:553–555PubMedCrossRefGoogle Scholar
  58. 58.
    Burgess P, Done HJ (1989) Adenocarcinoma of the appendix. J R Soc Med 82:28–29PubMedGoogle Scholar
  59. 59.
    Nielsen GP, Isaksson HJ, Finnbogason H, Gunnlaugsson GH (1991) Adenocarcinoma of the vermiform appendix. A population study. APMIS 99:653–656PubMedCrossRefGoogle Scholar
  60. 60.
    Uihlein A, McDonald JR (1943) Primary carcinoma of the appendix resembling carcinoma of the colon. Surg Gynecol Obstet 76:711–714Google Scholar
  61. 61.
    Steinberg M, Cohn I (1967) Primary adenocarcinoma of the appendix. Surgery 61:644–660PubMedGoogle Scholar
  62. 62.
    Wilson R (1962) Primary carcinoma of the appendix. Am J Surg 104:238–249PubMedCrossRefGoogle Scholar
  63. 63.
    Gamble HA (1976) Adenocarcinoma of the appendix: an unusual case and review. Dis Colon Rectum 19:621–625PubMedCrossRefGoogle Scholar
  64. 64.
    Hopkins BG, Tullis RH, Kristensen KAB (1973) Primary adenocarcinoma of the vermiform appendix: report of seven cases and review of the literature. Dis Colon Rectum 16:140–144PubMedCrossRefGoogle Scholar
  65. 65.
    Higa E, Rosai J, Pizzimbono CA, Wise L (1973) Mucosal hyperplasia, mucinous cystadenoma and mucinous cystadenocarcinoma of the appendix. Cancer 32:1525–1541PubMedCrossRefGoogle Scholar
  66. 66.
    McGregor JK, McGregor DD (1960) Adenocarcinoma of the appendix. Surgery 48:925–935Google Scholar
  67. 67.
    Sugarbaker PH, Kern K, Lack E (1987) Malignant pseudomyxoma peritonei of colonic origin. Dis Colon Rectum 30:772–779PubMedCrossRefGoogle Scholar
  68. 68.
    Wolff M, Ahmed N (1976) Epithelial neoplasms of the vermiform appendix (exclusion of carcinoid). Cancer 37:2493–2510PubMedCrossRefGoogle Scholar
  69. 69.
    Niceberg DM, Feldman S, Mandleberg A (1956) Adenocarcinoma of the vermiform appendix. A case presentation and review of the literature. Surgery 40:560–570PubMedGoogle Scholar
  70. 70.
    Hata K, Tanaka N, Nomura Y, Wada I, Nagawa H (2002) Early appendiceal adenocarcinoma. A review of the literature with special reference to optimal surgical procedures. J Gastroenterol 37:210–214PubMedCrossRefGoogle Scholar
  71. 71.
    Andersson A, Bergdahl L, Boquist L (1976) Primary carcinoma of the appendix. Ann Surg 183:53–57PubMedCrossRefGoogle Scholar
  72. 72.
    Sieracki JC, Tesluk H (1956) Primary adenocarcinoma of the vermiform appendix. Cancer 9:997–1011PubMedCrossRefGoogle Scholar
  73. 73.
    Sugarbaker PH (1991) Cytoreductive surgery and intraperitoneal chemotherapy with peritoneal spread of cytoadenocarcinoma. Eur J Surg Suppl 561:75–82PubMedGoogle Scholar
  74. 74.
    Lewin KJ, Ranchod M, Dorfman RF (1978) Lymphomas of the gastrointestinal tract. Cancer 42:693–707PubMedCrossRefGoogle Scholar
  75. 75.
    Contreary K, Nance FC, Becker VF (1980) Primary lymphoma of the gastrointestinal tract. Ann Surg 191:593–598PubMedCrossRefGoogle Scholar
  76. 76.
    Carpender BW (1991) Lymphoma of the appendix. Gastrointest Radiol 16:256–258CrossRefGoogle Scholar
  77. 77.
    D’Amore F, Brincker H, Grønbæk K, Thorling K, Pedersen M, Jensen MK (1994) Non-Hodgkin’s lymphoma of the gastrointestinal tract: a population-based analysis of incidence, geographic distribution, clinicopathologic presentation features, and prognosis. Danish Lymphoma Study Group. J Clin Oncol 12:1673–1684PubMedGoogle Scholar
  78. 78.
    Pascuale MD, Shabahang M, Bitterman P, Lack EE, Evans SRT (1994) Primary lymphoma of the appendix. Case report and review of the literature. Surg Oncol 3:243–248CrossRefGoogle Scholar
  79. 79.
    Kanavaros P (1998) Primary gastric peripheral T-cell malignant lymphoma with helper/inducer phenotype. First case report with a complete histological ultrastructural and immunohistochemical study. Cancer 61:1602–1610CrossRefGoogle Scholar
  80. 80.
    Moulbayed P (1987) T-cell lymphoma of the stomach: morphological and immunological studies characterizing two cases of T-cell lymphoma. Virchows Arch 411:523–529CrossRefGoogle Scholar
  81. 81.
    Kitamura Y, Ohta T, Terada T (2000) Primary T-cell non-Hodgkin’s malignant lymphoma of the appendix. Pathol Int 50:313–317PubMedCrossRefGoogle Scholar
  82. 82.
    Mori M, Kusunoki T, Kikunoki M, Motoori T, Sugimachi K (1985) Primary malignant lymphoma of the appendix. Jpn J Surg 15:230–233PubMedCrossRefGoogle Scholar
  83. 83.
    Sin IC, Ling ET, Prentice RSA (1980) Burkitt’s lymphoma of the appendix: report of two cases. Human Pathol 11:465–470CrossRefGoogle Scholar
  84. 84.
    Stewart RJ, Mirakhur M (1986) Primary malignant lymphoma of the appendix. Ulster Med J 55:187–189PubMedGoogle Scholar
  85. 85.
    Freeman C, Berg JW, Cutler SJ (1972) Occurrence and prognosis of extranodal lymphomas. Cancer 29:252–260PubMedCrossRefGoogle Scholar
  86. 86.
    Dawson IMP, Cornes JS, Morson BC (1961) Primary malignant lymphoid tumours of the intestinal tract. Report of 37 cases with a study of factors influencing prognosis. Br J Surg 49:80–89PubMedCrossRefGoogle Scholar
  87. 87.
    Uncu H, Erdem E, Tüzüner A (1998) Primary malignant lymphoma of the appendix: case report and review of the literature. Acta Chir Hung 37(1–2):11–16PubMedGoogle Scholar
  88. 88.
    Jones PA (1979) Leiomyosarcoma of the appendix: report of two cases. Dis Colon Rectum 22:175–178PubMedCrossRefGoogle Scholar
  89. 89.
    Michalany J, Galindo W (1973) Classification of neuromas of the appendix. Beitr Pathol 150:213–228PubMedGoogle Scholar
  90. 90.
    Zarabi M, LaBach JP (1982) Ganglioneuroma causing acute appendicitis. Hum Pathol 13:1143–1146PubMedGoogle Scholar
  91. 91.
    Deziel DJ, Saclarides TJ, Marshall JS, Yaremko LM (1991) Appendiceal Kaposi’s sarcoma: a cause of right lower quadrant pain in the acquired immunodeficiency syndrome. Am J Gastroenterol 86:901–903PubMedGoogle Scholar
  92. 92.
    Zebrowska G, Walsh NM (1991) Human immunodeficiency virus related Karposi’s sarcoma of the appendix and acute appendicitis. Report of a case and review of the literature. Arch Pathol Lab Med 115:1157–1160PubMedGoogle Scholar
  93. 93.
    Johnston J, Helwig EB (1981) Granular cell tumours of the gastrointestinal tract and perianal region: a study of 74 cases. Dig Dis Sci 26:807–816PubMedCrossRefGoogle Scholar
  94. 94.
    Bernhardt H, Young JM (1965) Mucocele and pseudomyxoma peritonei of appendiceal origin: clinicopathologic aspects. Am J Surg 109:235PubMedCrossRefGoogle Scholar
  95. 95.
    Burney RE, Koss N, Goldberg IS (1974) Acute appendicitis secondary to metastatic carcinoma of the breast. Arch Surg 108:872PubMedGoogle Scholar
  96. 96.
    Maddox PR (1990) Acute appendicitis secondary to metastatic carcinoma of the breast. Br J Clin Pract 44:376–378PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Mark E. O’Donnell
    • 1
    • 3
  • Stephen A. Badger
    • 1
  • Garth C. Beattie
    • 1
  • Jim Carson
    • 2
  • W. Ian H. Garstin
    • 1
  1. 1.Department of SurgeryAntrim Area HospitalAntrimUK
  2. 2.Department of HistopathologyAntrim Area HospitalAntrimUK
  3. 3.County DownUK

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