173
Views
0
CrossRef citations to date
0
Altmetric
Review

Understanding the increasing incidence of neuroendocrine tumors

, , &
Pages 377-385 | Received 24 Mar 2023, Accepted 13 Jul 2023, Published online: 19 Jul 2023

References

  • Gustafsson BI, Kidd M, Modlin IM. Neuroendocrine tumors of the diffuse neuroendocrine system. Curr Opin Oncol. 2008;20(1):1–12. doi: 10.1097/CCO.0b013e3282f1c595
  • Oronsky B, Ma PC, Morgensztern D, et al. Nothing but NET: a review of neuroendocrine tumors and carcinomas. Neoplasia. 2017;19(12):991–1002. doi: 10.1016/j.neo.2017.09.002
  • Dasari A, Shen C, Halperin D, et al. Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the United States. JAMA Oncol. 2017;3(10):1335–1342. doi: 10.1001/jamaoncol.2017.0589
  • Das S, Dasari A. Epidemiology, incidence, and prevalence of neuroendocrine neoplasms: are there global differences? Curr Oncol Rep. 2021;23(4):23. doi: 10.1007/s11912-021-01029-7
  • Leoncini E, Boffetta P, Shafir M, et al. Increased incidence trend of low-grade and high-grade neuroendocrine neoplasms. Endocrine. 2017;58(2):368–379. doi: 10.1007/s12020-017-1273-x
  • Huguet I, Grossman AB, O’Toole D, et al. Changes in the epidemiology of neuroendocrine tumours. Neuroendocrinology. 2017;104(2):105–111. doi: 10.1159/000441897
  • Fraenkel M, Kim M, Faggiano A, et al. Incidence of gastroenteropancreatic neuroendocrine tumours: a systematic review of the literature. Endocr Relat Cancer. 2014;21(3):R153–R163. doi: 10.1530/ERC-13-0125
  • Xu Z, Wang L, Dai S, et al. Epidemiologic trends of and factors associated with overall survival for patients with gastroenteropancreatic neuroendocrine tumors in the United States. JAMA Netw Open. 2021;4(9):4. doi: 10.1001/jamanetworkopen.2021.24750
  • White BE, Rous B, Chandrakumaran K, et al. Incidence and survival of neuroendocrine neoplasia in England 1995–2018: A retrospective, population-based study. Lancet Reg Heal - Eur. 2022;23:100510. doi: 10.1016/j.lanepe.2022.100510
  • Levi F, Te VC, Randimbison L, et al. Epidemiology of carcinoid neoplasms in Vaud, Switzerland, 1974–97. Br J Cancer. 2000;83(7):952–955. doi: 10.1054/bjoc.2000.1394
  • Alwan H, La Rosa S, Andreas Kopp P, et al. Incidence trends of lung and gastroenteropancreatic neuroendocrine neoplasms in Switzerland. Cancer Med. 2020;9(24):9454–9461. doi: 10.1002/cam4.3524
  • Niederle MB, Hackl M, Kaserer K, et al. Gastroenteropancreatic neuroendocrine tumours: the current incidence and staging based on the WHO and European Neuroendocrine Tumour Society classification: an analysis based on prospectively collected parameters. Endocr Relat Cancer. 2010;17(4):909–918. doi: 10.1677/ERC-10-0152
  • Hemminki KL, Li X. Incidence trends and risk factors of carcinoid tumors: a nationwide epidemiologic study from Sweden. Cancer. 2001; Oct 15;92(8):2204–2210. doi: 10.1002/1097-0142(20011015)92:8<2204:AID-CNCR1564>3.0.CO;2-R
  • Quaedvlieg PFHJ, Visser O, Lamers CBHW, et al. Epidemiology and survival in patients with carcinoid disease in the Netherlands. An epidemiological study with 2391 patients. Ann Oncol Off J Eur Soc Med Oncol. 2001;12(9):1295–1300. doi: 10.1023/A:1012272314550
  • Korse CM, Taal BG, Van Velthuysen MLF, et al. Incidence and survival of neuroendocrine tumours in the Netherlands according to histological grade: experience of two decades of cancer registry. Eur J Cancer. 2013;49(8):1975–1983. doi: 10.1016/j.ejca.2012.12.022
  • Lepage C, Bouvier AM, Phelip JM, et al. Incidence and management of malignant digestive endocrine tumours in a well defined French population. Gut. 2004;53:549–553. doi: 10.1136/gut.2003.026401
  • Hauso O, Gustafsson BI, Kidd M, et al. Neuroendocrine tumor epidemiology: contrasting Norway and North America. Cancer. 2008;113(10):2655–2664. doi: 10.1002/cncr.23883
  • Cetinkaya RB, Aagnes B, Thiis-Evensen E, et al. Trends in incidence of neuroendocrine neoplasms in Norway: a report of 16,075 cases from 1993 through 2010. Neuroendocrinology. 2017;104(1):1–10. doi: 10.1159/000442207
  • Kaçmaz E, Sarasqueta AF, van Eeden S, et al. Update on incidence, prevalence, treatment and survival of patients with small bowel neuroendocrine neoplasms in the Netherlands. World J Surg. 2021;45(8):2482–2491. doi: 10.1007/s00268-021-06119-y
  • Hoej LB, Nykjær KM, Gronbaek H. Incidence and survival of patients with small intestinal neuroendocrine tumours in a Danish NET center. ScientificWorldjournal. 2012;2012:1–7. doi: 10.1100/2012/206350
  • Ellis L, Shale MJ, Coleman MP. Carcinoid tumors of the gastrointestinal tract: trends in incidence in England since 1971. Am J Gastroenterol. 2010;105(12):2563–2569. doi: 10.1038/ajg.2010.341
  • Caldarella A, Crocetti E, Paci E. Distribution, incidence, and prognosis in neuroendocrine tumors: a population based study from a cancer registry. Pathol Oncol Res. 2011;17(3):759–763. doi: 10.1007/s12253-011-9382-y
  • Fanello S, Mangone L, Sacchettini C, et al. Variety of hormones produced by rare neuroendocrine tumors (NETs): examination of epidemiology and prognostic factors for NETs in Italy. 2016;34:e15656–e15656. doi: 10.1200/JCO20163415suppl.e15656
  • Scherübl H, Streller B, Stabenow R, et al. Clinically detected gastroenteropancreatic neuroendocrine tumors are on the rise: epidemiological changes in Germany. World J Gastroenterol. 2013;19(47):9012–9019. doi: 10.3748/wjg.v19.i47.9012
  • Gudmundsdottir H, Möller PH, Jonasson JG, et al. Gastroenteropancreatic neuroendocrine tumors in Iceland: a population-based study. Scand J Gastroenterol. 2019;54(1):69–75. doi: 10.1080/00365521.2018.1553061
  • Luke C, Price T, Townsend A, et al. Epidemiology of neuroendocrine cancers in an Australian population. Cancer Causes Control. 2010;21(6):931–938. doi: 10.1007/s10552-010-9519-4
  • Michael M, Thursfield V, Te Marvelde L, et al. Incidence, prevalence, and survival trends for neuroendocrine neoplasms in Victoria, Australia, from 1982 to 2019: based on site, grade, and region. Asia Pac J Clin Oncol. 2022;18(5):e306–e317. doi: 10.1111/ajco.13671
  • Wyld D, Moore J, Tran N, et al. Incidence, survival and stage at diagnosis of small intestinal neuroendocrine tumours in Queensland, Australia, 2001-2015. Asia‐Pac J Clin Oncol. 2021;17(4):350–358. doi: 10.1111/ajco.13503
  • Ito T, Igarashi H, Nakamura K, et al. Epidemiological trends of pancreatic and gastrointestinal neuroendocrine tumors in Japan: a nationwide survey analysis. J Gastroenterol. 2015;50(1):58–64. doi: 10.1007/s00535-014-0934-2
  • Soga J. Early-stage carcinoids of the gastrointestinal tract: an analysis of 1914 reported cases. Cancer. 2005;103(8):1587–1595. doi: 10.1002/cncr.20939
  • Cho MY, Kim JM, Sohn JH, et al. Current trends of the incidence and pathological diagnosis of gastroenteropancreatic neuroendocrine tumors (GEP-NETs) in Korea 2000-2009: multicenter study. Cancer Res Treat. 2012;44(3):157–165. doi: 10.4143/crt.2012.44.3.157
  • Tsai HJ, Wu CC, Tsai CR, et al. The epidemiology of neuroendocrine tumors in Taiwan: a nation-wide cancer registry-based study. PLoS One. 2013;8(4):e62487. doi: 10.1371/journal.pone.0062487
  • Chang JS, Chen LT, Shan YS, et al. An updated analysis of the epidemiologic trends of neuroendocrine tumors in Taiwan. Sci Rep. 2021;11(1):11. doi: 10.1038/s41598-021-86839-2
  • Fan JH, Zhang YQ, Shi SS, et al. A nation-wide retrospective epidemiological study of gastroenteropancreatic neuroendocrine neoplasms in china. Oncotarget. 2017;8(42):71699–71708. doi: 10.18632/oncotarget.17599
  • Zhang M, Zhao P, Shi X, et al. Clinicopathological features and prognosis of gastroenteropancreatic neuroendocrine neoplasms in a Chinese population: a large, retrospective single-centre study. BMC Endocr Disord. 2017;17(1):17. doi: 10.1186/s12902-017-0190-6
  • Wu L, Fu J, Wan L, et al. Survival outcomes and surgical intervention of small intestinal neuroendocrine tumors: a population based retrospective study. Oncotarget. 2017;8(3):4935–4947. doi: 10.18632/oncotarget.13632
  • Cukier M, Law C, Liu N, et al. Epidemiology and survival of neuroendocrine tumors in Ontario: a 15-year population-based study. 2012;30:184–184. doi: 10.1200/jco2012304_suppl184
  • Yao JC, Hassan M, Phan A, 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(18):3063–3072. doi: 10.1200/JCO.2007.15.4377
  • Maggard MA, O’Connell JB, Ko CY. Updated population-based review of carcinoid tumors. Ann Surg. 2004;240(1):117–122. doi: 10.1097/01.sla.0000129342.67174.67
  • Halfdanarson TR, Rabe KG, Rubin J, et al. Pancreatic neuroendocrine tumors (PNETs): incidence, prognosis and recent trend toward improved survival. Ann Oncol Off J Eur Soc Med Oncol. 2008;19(10):1727–1733. doi: 10.1093/annonc/mdn351
  • Sonbol MB, Mazza GL, Mi L, et al. Survival and incidence patterns of pancreatic neuroendocrine tumors over the last 2 decades: a SEER database analysis. Oncology. 2022;27(7):573. doi: 10.1093/oncolo/oyac049
  • Lawrence B, Gustafsson BI, Chan A, et al. The epidemiology of gastroenteropancreatic neuroendocrine tumors. Endocrinol Metab Clin North Am. 2011;40(1):1–18. doi: 10.1016/j.ecl.2010.12.005
  • Tsikitis VL, Wertheim BC, Guerrero MA. Trends of incidence and survival of gastrointestinal neuroendocrine tumors in the United States: a Seer analysis. J Cancer. 2012;3:292–302. doi: 10.7150/jca.4502
  • Balmadrid BL, Thomas CM, Coffman CJ, et al. Factors associated with survival of veterans with gastrointestinal neuroendocrine tumors. J Cancer Epidemiol. 2012;2012:1–5. doi: 10.1155/2012/986708
  • Abdel-Rahman O, Ghosh S. A real-world study of the incidence and outcomes of early-onset well-differentiated neuroendocrine neoplasms. Am J Clin Oncol. 2022;45(8):338–343. doi: 10.1097/COC.0000000000000925
  • Wang J, Liu J, He C, et al. Trends in incidence and survival of patients with pancreatic neuroendocrine neoplasm, 1987–2016. J Oncol. 2021;2021:1–11. doi: 10.1155/2021/4302675
  • Giraldi L, Vecchioni A, Carioli G, et al. Risk factors for pancreas and lung neuroendocrine neoplasms: a case–control study. Endocrine. 2021;71(1):233–241. doi: 10.1007/s12020-020-02464-5
  • Hiripi E, Bermejo JL, Sundquist J, et al. Familial gastrointestinal carcinoid tumours and associated cancers. Ann Oncol Off J Eur Soc Med Oncol. 2009;20(5):950–954. doi: 10.1093/annonc/mdn706
  • Neklason DW, Van Derslice J, Curtin K, et al. Evidence for a heritable contribution to neuroendocrine tumors of the small intestine. Endocr Relat Cancer. 2016;23(2):93–100. doi: 10.1530/ERC-15-0442
  • Hemminki K, Li X. Familial carcinoid tumors and subsequent cancers: a nation-wide epidemiologic study from Sweden. Int J Cancer. 2001;94(3):444–448. doi: 10.1002/ijc.1473
  • Kharazmi E, Pukkala E, Sundquist K, et al. Familial risk of small intestinal carcinoid and adenocarcinoma. Clin Gastroenterol Hepatol. 2013;11(8):944–949. doi: 10.1016/j.cgh.2013.02.025
  • Faggiano A, Ferolla P, Grimaldi F, et al. Natural history of gastro-entero-pancreatic and thoracic neuroendocrine tumors. Data from a large prospective and retrospective Italian epidemiological study: the NET management study. J Endocrinol Invest. 2012;35(9):817–823. doi: 10.3275/8102
  • Perez K, Kulke MH, Chittenden A, et al. Clinical implications of pathogenic germline variants in small intestine neuroendocrine tumors (SI-NETs). JCO Precis Oncol. 2021;5(5):808–816. doi: 10.1200/PO.21.00047
  • Bassam SM, Zane AS, Golafshar M, et al. Germline cancer testing in unselected patients with neuroendocrine neoplasms: a multi-center prospective study. Endocr Abstr. 2022;89(10). doi:10.1530/endoabs.89.O10
  • Scarpa A, Chang DK, Nones K, et al. Whole-genome landscape of pancreatic neuroendocrine tumours. Nature. 2017;543(7643):65–71. doi: 10.1038/nature21063
  • Ter-Minassian M, Wang Z, Asomaning K, et al. Genetic associations with sporadic neuroendocrine tumor risk. Carcinogenesis. 2011;32(8):1216–1222. doi: 10.1093/carcin/bgr095
  • Sei Y, Zhao X, Forbes J, et al. A hereditary form of small intestinal carcinoid associated with a germline mutation in inositol polyphosphate multikinase. Gastroenterology. 2015;149(1):67–78. doi: 10.1053/j.gastro.2015.04.008
  • Shen C, Gu D, Zhou S, et al. Racial differences in the incidence and survival of patients with neuroendocrine tumors. Pancreas. 2019;48(10):1373–1379. doi: 10.1097/MPA.0000000000001431
  • Sarshekeh AM, Gu D, Zhou S, et al. Racial differences in the incidence and survival of patients with neuroendocrine tumors (NETs). 2018;36:e16175–e16175. doi: 10.1200/JCO20183615_suppl.e16175
  • Kaerlev L, Teglbjaerg PS, Sabroe S, et al. Occupational risk factors for small bowel carcinoid tumor: a European population-based case-control study. Journal Of Occupational & Environmental Medicine. 2002;44(6):516–522. doi: 10.1097/00043764-200206000-00012
  • VanDerslice J, Taddie MC, Curtin K, et al. Early life exposures associated with risk of small intestinal neuroendocrine tumors. PLoS One. 2020;15(4):15. doi: 10.1371/journal.pone.0231991
  • Hassan MM, Phan A, Li D, et al. Risk factors associated with neuroendocrine tumors: a U.S.-based case-control study. Int J Cancer. 2008;123(4):867–873. doi: 10.1002/ijc.23529
  • Feola T, Puliani G, Sesti F, et al. Risk factors for gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs): a three-centric case–control study. J Endocrinol Invest. 2022;45(4):849–857. doi: 10.1007/s40618-021-01715-0
  • Leoncini E, Carioli G, La Vecchia C, et al. Risk factors for neuroendocrine neoplasms: a systematic review and meta-analysis. Ann Oncol Off J Eur Soc Med Oncol. 2016;27(1):68–81. doi: 10.1093/annonc/mdv505
  • Rinzivillo M, Capurso G, Campana D, et al. Risk and protective factors for small intestine neuroendocrine tumors: a prospective case-control study. Neuroendocrinology. 2016;103(5):531–537. doi: 10.1159/000440884
  • Curtin K, Cannon-Albright LA, Van Derslice J, et al. Associations of tobacco and alcohol use with risk of neuroendocrine tumors of the small intestine in Utah. Cancer Epidemiol Biomarkers Prev. 2019;28:p. 1998.
  • 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(1):27–34. doi: 10.1023/A:1013922226614
  • Schneider JL, Kolitsopoulos F, Corley DA. Risk of gastric cancer, gastrointestinal cancers and other cancers: a comparison of treatment with pantoprazole and other proton pump inhibitors. Aliment Pharmacol Ther. 2016;43(1):73–82. doi: 10.1111/apt.13450
  • 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. doi: 10.1002/ibd.20172
  • Yu J, Refsum E, Perrin V, et al. Inflammatory bowel disease and risk of adenocarcinoma and neuroendocrine tumors in the small bowel. Ann Oncol Off J Eur Soc Med Oncol. 2022;33(6):649–656. doi: 10.1016/j.annonc.2022.02.226
  • Emilsson L, Semrad C, Lebwohl B, et al. Risk of small bowel adenocarcinoma, adenomas, and carcinoids in a nationwide cohort of individuals with celiac disease. Gastroenterology. 2020;159(5):1686–1694.e2. doi: 10.1053/j.gastro.2020.07.007
  • McCarthy DM. Proton pump inhibitor use, hypergastrinemia, and gastric carcinoids—What is the relationship? Int J Mol Sci. 2020;21(2):662. doi: 10.3390/ijms21020662
  • Lundell L, Vieth M, Gibson F, et al. Systematic review: the effects of long-term proton pump inhibitor use on serum gastrin levels and gastric histology. Aliment Pharmacol Ther. 2015;42(6):649–663. doi: 10.1111/apt.13324
  • Brenna E, Waldum HL. Trophic effect of gastrin on the enterochromaffin like cells of the rat stomach: establishment of a dose response relationship. Gut. 1992;33(10):1303–1306. doi: 10.1136/gut.33.10.1303
  • Modlin IM, Lye KD, Kidd M. A 50-year analysis of 562 gastric carcinoids: small tumor or larger problem? Am J Gastroenterol. 2004;99(1):23–32. doi: 10.1046/j.1572-0241.2003.04027.x
  • Modlin IM, Lye KD, Kidd M. A 5-decade analysis of 13,715 carcinoid tumors. Cancer. 2003;97(4):934–959. doi: 10.1002/cncr.11105
  • Ramachandran A, Madhusudhan KS. Advances in the imaging of gastroenteropancreatic neuroendocrine neoplasms. World J Gastroenterol. 2022;28(26):3008–3026. doi: 10.3748/wjg.v28.i26.3008
  • Ebbehoj A, Li D, Kaur RJ, et al. Epidemiology of adrenal tumors - a population-based study in Olmsted County. Minnesota Lancet Diabetes Endocrinol. 2020;8(11):894. doi: 10.1016/S2213-8587(20)30314-4
  • Hallet J, Law CHL, Cukier M, et al. Exploring the rising incidence of neuroendocrine tumors: a population-based analysis of epidemiology, metastatic presentation, and outcomes. Cancer. 2015;121(4):589–597. doi: 10.1002/cncr.29099
  • Kuo EJ, Salem RR. Population-level analysis of pancreatic neuroendocrine tumors 2 cm or less in size. Ann Surg Oncol. 2013;20(9):2815–2821. doi: 10.1245/s10434-013-3005-7
  • Sonbol MB, Mazza GL, Mi L, et al. Survival and incidence patterns of pancreatic neuroendocrine tumors over the last 2 decades: a SEER database analysis. Oncology. 2022;27(7):573–578. doi: 10.1093/oncolo/oyac049
  • Scherübl H, Cadiot G. Early gastroenteropancreatic neuroendocrine tumors: endoscopic therapy and surveillance. Visc Med. 2017;33(5):332–338. doi: 10.1159/000459404
  • Hscherüb P, Klöppel C. Neuroendokrine Neoplasien des Rektums auf dem Vormarsch – ein Update. Z Gastroenterol. 2009;47(4):365–371. doi: 10.1055/s-2008-1027930
  • Stasinos I, Kamperidis N, Murino A, et al. Single incision laparoscopic assisted double balloon enteroscopy: a novel technique to manage small bowel pathology. Surg Endosc. 2020;34(6):2773–2779. doi: 10.1007/s00464-020-07446-2
  • Rossi RE, Elli L, Branchi F, et al. Double-balloon enteroscopy in detecting small-bowel neuroendocrine neoplasms: a single-center prospective study. Digestion. 2021;102(5):722–730. doi: 10.1159/000511850
  • Rossi RE, Elvevi A, Gallo C, et al. Endoscopic techniques for diagnosis and treatment of gastro-entero-pancreatic neuroendocrine neoplasms: where we are. World J Gastroenterol. 2022;28(26):3258–3273. doi: 10.3748/wjg.v28.i26.3258
  • Nguyen AH, O’Leary MP, De Andrade JP, et al. Presentation and survival of gastro-entero-pancreatic neuroendocrine tumors in young adults versus older patients. Am J Surg. 2022;223(5):939–944. doi: 10.1016/j.amjsurg.2021.08.030
  • Goksu SY, Ozer M, Kazmi SMA, et al. Distinct clinical characteristics in young-onset pancreatic neuroendocrine tumor. Cancers (Basel). 2020;12(9):2501–2515. doi: 10.3390/cancers12092501
  • Chauhan A, Yu Q, Ray N, et al. Global burden of neuroendocrine tumors and changing incidence in Kentucky. Oncotarget. 2018;9(27):19245–19254. doi: 10.18632/oncotarget.24983
  • Scoazec JY, Couvelard A. Classification des tumeurs neuroendocrines pancréatiques : nouveautés introduites par la classification OMS 2017 des tumeurs des organes endocrines et perspectives. Ann Pathol. 2017;37(6):444–456. doi: 10.1016/j.annpat.2017.10.003
  • Assarzadegan N, Montgomery E. What is new in the 2019 World Health Organization (WHO) classification of tumors of the digestive system: review of selected updates on neuroendocrine neoplasms, appendiceal tumors, and molecular testing. Arch Pathol Lab Med. 2021;145(6):664–677. doi: 10.5858/arpa.2019-0665-RA
  • Manasanch EE, Smith JK, Bodnari A, et al. Tumor registry versus physician medical record review: a direct comparison of patients with pancreatic neuroendocrine tumors. J Oncol Pract. 2011;7(2):111–116. doi: 10.1200/JOP.2010.000097
  • Koizumi T, Otsuki K, Tanaka Y, et al. Epidemiology of neuroendocrine neoplasmas in Japan: based on analysis of hospital-based cancer registry data, 2009 –2015. BMC Endocr Disord. 2022;22(1):22. doi: 10.1186/s12902-022-01016-4
  • Heidsma CM, Engelsman AF, Van Dieren S, et al. Watchful waiting for small non-functional pancreatic neuroendocrine tumours: nationwide prospective cohort study (PANDORA). Br J Surg. 2021;108(8):888–891. doi: 10.1093/bjs/znab088
  • Soares HP, Guthrie KA, Ahmad SA, et al. Randomized phase II trial of postoperative adjuvant capecitabine and temozolomide versus observation in high-risk pancreatic neuroendocrine tumors: SWOG S2104. 2022;40:TPS515–TPS515. doi: 10.1200/JCO2022404_supplTPS515
  • Strosberg J, El-Haddad G, Wolin E, et al. Phase 3 trial of 177 Lu-dotatate for midgut neuroendocrine tumors. N Engl J Med. 2017;376(2):125–135. doi: 10.1056/NEJMoa1607427
  • Raymond E, Dahan L, Raoul J-L, et al. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med. 2011;364(6):501–513. doi: 10.1056/NEJMoa1003825

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.