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Prevalence of Small Intestine Carcinoid Tumors: A US Population-Based Study 2012–2017

Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Background and Aims

Most carcinoid tumors of the gastrointestinal tract are located in the small bowel (SB). Epidemiological studies of these tumors have been limited by small sample sizes. Our aim was to evaluate the epidemiology of SB carcinoids (SBCs) using a large database.

Methods

We queried a commercial database (Explorys), an aggregate of electronic health data from 26 US healthcare systems. We identified patients with SBCs between 2012 and 2017. We evaluated the epidemiology of SBC and identified possible risk factors.

Results

Of the 35,798,290 individuals in the database between 2012 and 2017, we identified 3280 patients with SBCs, with a prevalence of 9.2/100,000. Prevalence was higher in men [odds ratio (OR) 1.23, 95% confidence interval (CI) 1.153–1.322, p < 0.0001], whites [OR 2.031, 95% CI 1.872–2.203, p < 0.0001], and elderly (aged > 65) [OR 4.856, 95% CI 4.533–5.203, p < 0.0001]. Patients with SBCs were more likely to have a history of smoking [OR 2.749, 95% CI 2.549–2.970, p < 0.0001], alcohol use [OR 2.031, 95% CI 1.864–2.21, p < 0.0001], obesity (BMI > 30) [OR 3.476, 95% CI 3.213–3.761, p < 0.0001], diabetes mellitus [OR 4.198, 95% CI 3.900–4.519, p < 0.0001], and a family history of cancer [OR 5.902, 95% CI 5.396–6.456, p < 0.0001].

Conclusions

This is one of the largest studies done on the prevalence of SBC. The prevalence of 9.2/100,000 individuals is higher than previously reported. Further genetic and environmental studies are needed to understand the potential mechanisms for the risk factors identified in this study.

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Abbreviations

BMI:

Body mass index

CD:

Crohn’s disease

CI:

Confidence interval

DM:

Diabetes mellitus

EHR:

Electronic health record

FTT:

Failure to thrive

GI:

Gastrointestinal

HDG:

Health data gateway

HIPAA:

Health Insurance Portability and Accountability Act

IBD:

Inflammatory bowel disease

IRB:

Institutional review board

MEN1:

Multiple endocrine neoplasia type 1

NCI:

National Cancer Institute

NET:

Neuroendocrine tumor

OR:

Odds ratio

SB:

Small bowel

SBC:

Small bowel carcinoid

SEER:

Surveillance, Epidemiology, and End Results

SNOMED-CT:

Systematized Nomenclature of Medicine-Clinical Terms

UC:

Ulcerative colitis

US:

United States

References

  1. Lawrence B, Gustafsson BI, Chan A, et al. The epidemiology of gastroenteropancreatic neuroendocrine tumors. Endocrinol Metab Clin North Am. 2011;40:1–18.

    Article  PubMed  Google Scholar 

  2. Klimstra DS, Modlin IR, Coppola D, et al. The pathologic classification of neuroendocrine tumors: a review of nomenclature, grading, and staging systems. Pancreas. 2010;39:707–712.

    Article  PubMed  Google Scholar 

  3. KlÖppel G, Perren A, Heitz PU. The gastroenteropancreatic neuroendocrine cell system and its tumors: the WHO classification. Ann N Y Acad Sci. 2004;1014:13–27.

    Article  PubMed  Google Scholar 

  4. Caplin ME, Buscombe JR, Hilson AJ, et al. Carcinoid tumour. The Lancet. 1998;352:799–805.

    Article  CAS  Google Scholar 

  5. Kulke MH, Mayer RJ. Carcinoid tumors. N Engl J Med. 1999;340:858–868.

    Article  CAS  PubMed  Google Scholar 

  6. von der Ohe MR, Michael C, Larry KK, et al. Motor dysfunction of the small bowel and colon in patients with the carcinoid syndrome and diarrhea. N Engl J Med. 1993;329:1073–1078.

    Article  PubMed  Google Scholar 

  7. Maton PN. The carcinoid syndrome. JAMA. 1988;260:1602–1605.

    Article  CAS  PubMed  Google Scholar 

  8. Pellikka PA, Tajik AJ, Khandheria BK, et al. Carcinoid heart disease. Clinical and echocardiographic spectrum in 74 patients. Circulation. 1993;87:1188–1196.

    Article  CAS  PubMed  Google Scholar 

  9. Yao JC, Hassan M, Phan A, Dagohoy C, et al. One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26:3063–3072.

    Article  PubMed  Google Scholar 

  10. Modlin IM, Lye KD, Kidd M. A 5-decade analysis of 13,715 carcinoid tumors. Cancer. 2003;97:934–959.

    Article  PubMed  Google Scholar 

  11. Modlin IM, Sandor A. An analysis of 8305 cases of carcinoid tumors. Cancer. 1997;79:813–829.

    Article  CAS  PubMed  Google Scholar 

  12. Godwin JD. Carcinoid tumors: an analysis of 2837 cases. Cancer. 1975;36:560–569.

    Article  PubMed  Google Scholar 

  13. Barclay THC, Schapira DV. Malignant tumors of the small intestine. Cancer. 1983;51:878–881.

    Article  CAS  PubMed  Google Scholar 

  14. Hemminki K, Li X. Incidence trends and risk factors of carcinoid tumors. Cancer. 2001;92:2204–2210.

    Article  CAS  PubMed  Google Scholar 

  15. Norheim I, Oberg K, Theodorsson-Norheim E, et al. Malignant carcinoid tumors. An analysis of 103 patients with regard to tumor localization, hormone production, and survival. Ann Surg. 1987;206:115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Quaedvlieg PF, Visser O, Lamers CB, et al. Epidemiology and survival in patients with carcinoid disease in the Netherlands: an epidemiological study with 2391 patients. Ann Oncol. 2001;12:1295–1300.

    Article  CAS  PubMed  Google Scholar 

  17. Uhr JH, Shah J, Warner RR, et al. Racial disparities in clinical presentation and surgical outcomes in patients with small bowel carcinoid tumors. Am Surg. 2016;82:E89.

    PubMed  Google Scholar 

  18. Bilimoria KY, Bentrem DJ, Wayne JD, et al. Small bowel cancer in the United States: changes in epidemiology, treatment, and survival over the last 20 years. Ann Surg. 2009;249:63–71.

    Article  PubMed  Google Scholar 

  19. Kaerlev L, Teglbjaerg PS, Sabroe S, et al. The importance of smoking and medical history for development of small bowel carcinoid tumor: a European population-based case–control Study. Cancer Causes Control. 2002;13:27–34.

    Article  PubMed  Google Scholar 

  20. Hatzaras I, Palesty JA, Abir F, et al. Small-bowel tumors: epidemiologic and clinical characteristics of 1260 cases from the Connecticut tumor registry. Arch Surg. 2007;142:229–235.

    Article  PubMed  Google Scholar 

  21. Taal BG, Visser O. Epidemiology of neuroendocrine tumours. Neuroendocrinology. 2004;80:3–7.

    Article  CAS  PubMed  Google Scholar 

  22. Haselkorn T, Whittemore AS, Lilienfeld DE. Incidence of small bowel cancer in the United States and worldwide: geographic, temporal, and racial differences. Cancer Causes Control. 2005;16:781–787.

    Article  PubMed  Google Scholar 

  23. Neugut AI, Jacobson JS, Suh S, et al. The epidemiology of cancer of the small bowel. Cancer Epidemiol Prev Biomark. 1998;7:243–251.

    CAS  Google Scholar 

  24. Seydafkan S, Coppola D. Neuroendocrine neoplasms of the small intestine. In: Nasir A, Coppola D, eds. Neuroendocrine Tumors: Review of Pathology, Molecular and Therapeutic Advances. New York: Springer; 2016:273–288.

    Chapter  Google Scholar 

  25. Mocellin S, Nitti D. Gastrointestinal carcinoid: epidemiological and survival evidence from a large population-based study (n = 25 531). Ann Oncol. 2013;24:3040–3044.

    Article  CAS  PubMed  Google Scholar 

  26. Maggard MA, O’Connell JB, Ko CY. Updated population-based review of carcinoid tumors. Ann Surg. 2004;240:117.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Naef M, Bühlmann M, Baer HU. Small bowel tumors: diagnosis, therapy and prognostic factors. Langenbeck’s Arch Surg. 1999;384:176–180.

    Article  CAS  Google Scholar 

  28. Chow WH, Linet MS, McLaughlin JK, et al. Risk factors for small intestine cancer. Cancer Causes Control. 1993;4:163–169.

    Article  CAS  PubMed  Google Scholar 

  29. Wu AH, Yu MC, Mack TM. Smoking, alcohol use, dietary factors and risk of small intestinal adenocarcinoma. Int J Cancer. 1997;70:512–517.

    Article  CAS  PubMed  Google Scholar 

  30. Leoncini E, Carioli G, La Vecchia C, et al. Risk factors for neuroendocrine neoplasms: a systematic review and meta-analysis. Ann Oncol. 2015;27:68–81.

    Article  PubMed  Google Scholar 

  31. Cross AJ, Leitzmann MF, Subar AF, et al. Prospective study of meat and fat intake in relation to small intestinal cancer. Can Res. 2008;68:9274–9279.

    Article  CAS  Google Scholar 

  32. Explorys Team. We unlock the power of BIG DATA to improve healthcare for everyone. Explorys 2015. https://www.explorys.com/about-us.html. Accessed August 25, 2016.

  33. Vollset SE. Confidence intervals for a binomial proportion. Stat Med. 1993;12:809–824.

    Article  CAS  PubMed  Google Scholar 

  34. MedCalc Software Team. Odds ratio calculator. MedCalc 2017. https://www.medcalc.org/calc/odds_ratio.php. Accessed October 2, 2017.

  35. Scosyrev E, Messing J, Noyes K, Veazie P, et al. Surveillance Epidemiology and End Results (SEER) program and population-based research in urologic oncology: an overview. Urol Oncol. 2012;30:126–132.

    Article  PubMed  Google Scholar 

  36. Makridis C, Öberg K, Juhlin C, et al. Surgical treatment of mid-gut carcinoid tumors. World J Surg. 1990;14:377–383.

    Article  CAS  PubMed  Google Scholar 

  37. Kulke MH, Freed E, Chiang DY, et al. High-resolution analysis of genetic alterations in small bowel carcinoid tumors reveals areas of recurrent amplification and loss. Genes Chromosom Cancer. 2008;47:591–603.

    Article  CAS  PubMed  Google Scholar 

  38. Hassan MM, Phan A, Li D, et al. Risk factors associated with neuroendocrine tumors: a US-based case–control study. Int J Cancer. 2008;123:867–873.

    Article  CAS  PubMed  Google Scholar 

  39. Teh BT, McArdle J, Chan SP, et al. Clinicopathologic studies of thymic carcinoids in multiple endocrine neoplasia Type 1. Medicine. 1997;76:21–29.

    Article  CAS  PubMed  Google Scholar 

  40. Goudet P, Murat A, Cardot-Bauters C, et al. Thymic neuroendocrine tumors in multiple endocrine neoplasia type 1: a comparative study on 21 cases among a series of 761 MEN1 from the GTE (Groupe des Tumeurs Endocrines). World J Surg. 2009;33:1197–1207.

    Article  PubMed  Google Scholar 

  41. Berna MJ, Annibale B, Marignani M, et al. Prospective study of gastric carcinoids and enterochromaffin-like cell changes in multiple endocrine neoplasia Type 1 and Zollinger–Ellison syndrome: identification of risk factors. J Clin Endocrinol Metab. 2008;93:1582–1591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Babovic-Vuksanovic D, Constantinou CL, Rubin J, et al. Familial occurrence of carcinoid tumors and association with other malignant neoplasms. Cancer Epidemiol Prev Biomark. 1999;8:715–719.

    CAS  Google Scholar 

  43. West NE, Wise PE, Herline AJ, et al. Carcinoid tumors are 15 times more common in patients with Crohn’s disease. Inflamm Bowel Dis. 2007;13:1129–1134.

    Article  CAS  PubMed  Google Scholar 

  44. Kaerlev L, Teglbjaerg PS, Sabroe S, et al. Occupational risk factors for small bowel carcinoid tumor: a European population-based case–control study. J Occup Environ Med. 2002;44:516–522.

    Article  CAS  PubMed  Google Scholar 

  45. Nadkarni PM, Darer JA. Migrating existing clinical content from ICD-9 to SNOMED. J Am Med Inform Assoc. 2010;17:602–607.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Mansoor E, Saleh MA, Cooper GS. Prevalence of eosinophilic gastroenteritis and colitis in a population-based study, from 2012 to 2017. Clin Gastroenterol Hepatol. 2017;15:1733–1741.

    Article  PubMed  Google Scholar 

  47. Kaelber DC, Foster W, Gilder J, et al. Patient characteristics associated with venous thromboembolic events: a cohort study using pooled electronic health record data. J Am Med Inform Assoc. 2012;19:965–972.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Chouhan V, Mansoor E, Parasa S, Cooper GS. Rates of prevalent colorectal cancer occurrence in persons 75 Years of age and older: a population-based national study. Dig Dis Sci. 2018;63:1–8. https://doi.org/10.1007/s10620-018-5073-9.

    Article  Google Scholar 

  49. Al-Kindi SG, Oliveira GH. Prevalence of preexisting cardiovascular disease in patients with different types of cancer: the unmet need for onco-cardiology. Mayo Clin Proc. 2016;91:81–83.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

Authors

Contributions

MAS, EM, and MA were involved in study conception and design; MAS and EM contributed to acquisition of data; MAS, EM, and GI analysed and interpreted the data; MAS, EM, MA, and GI drafted the manuscript; GI was involved in critical revision; MAS and EM were involved in statistical analysis; GI supervised the study.

Corresponding author

Correspondence to Gerard Isenberg.

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The authors declare that they have no conflict of interest.

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Abou Saleh, M., Mansoor, E., Anindo, M. et al. Prevalence of Small Intestine Carcinoid Tumors: A US Population-Based Study 2012–2017. Dig Dis Sci 64, 1328–1334 (2019). https://doi.org/10.1007/s10620-018-5402-z

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  • DOI: https://doi.org/10.1007/s10620-018-5402-z

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