Sex differences in carcinoid syndrome: A gap to be closed.


Journal

Reviews in endocrine & metabolic disorders
ISSN: 1573-2606
Titre abrégé: Rev Endocr Metab Disord
Pays: Germany
ID NLM: 100940588

Informations de publication

Date de publication:
06 2022
Historique:
accepted: 04 03 2022
pubmed: 17 3 2022
medline: 3 6 2022
entrez: 16 3 2022
Statut: ppublish

Résumé

The incidence of neuroendocrine neoplasms and related carcinoid syndrome (CS) has markedly increased over the last decades and women seem to be more at risk than men for developing CS. Nevertheless, very few studies have investigated sex differences in clinical presentation and outcomes of CS. However, as per other tumours, sex might be relevant in influencing tumour localization, delay in diagnosis, clinical outcomes, prognosis and overall survival in CS. The present review was aimed at evaluating sex differences in CS, as they emerge from an extensive search of the recent literature. It emerged that CS occurs more frequently in female than in male patients with NENs and women seem to have a better prognosis and a slight advantage in overall survival and response to therapy. Moreover, the disease likely impacts differently the quality of life of men and women, with different psychological and social consequences. Nevertheless, sex differences, even if partially known, are deeply underestimated in clinical practice and data from clinical trials are lacking. There is urgent need to increase our understanding of the sex-related differences of CS, in order to define tailored strategies of management of the disease, improving both the quality of life and the prognosis of affected patients.

Identifiants

pubmed: 35292889
doi: 10.1007/s11154-022-09719-8
pii: 10.1007/s11154-022-09719-8
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

659-669

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Baggio G, Corsini A, Floreani A, Giannini S, Zagonel V. Gender medicine: a task for the third millennium. Clin Chem Lab Med. 2013;51(4):713–27.
pubmed: 23515103 doi: 10.1515/cclm-2012-0849
Oertelt-Prigione S. The influence of sex and gender on the immune response. Autoimmun Rev. 2012;11(6–7):A479–85.
pubmed: 22155201 doi: 10.1016/j.autrev.2011.11.022
Dorak MT, Karpuzoglu E. Gender differences in cancer susceptibility: an inadequately addressed issue. Front Genet. 2012;3:268.
pubmed: 23226157 pmcid: 3508426 doi: 10.3389/fgene.2012.00268
Mogl MT, Dobrindt EM, Buschermöhle J, Bures C, Pratschke J, Amthauer H, et al. Influence of gender on therapy and outcome of neuroendocrine tumors of gastroenteropancreatic origin: a single-center analysis. Visc Med. 2020;36(1):20–7.
pubmed: 32110653 pmcid: 7036565 doi: 10.1159/000505500
Muscogiuri G, Altieri B, Albertelli M, Dotto A, Modica R, Barrea L, et al. Epidemiology of pancreatic neuroendocrine neoplasms: a gender perspective. Endocrine. 2020;69(2):441–50.
pubmed: 32468269 doi: 10.1007/s12020-020-02331-3
Muscogiuri G, Barrea L, Feola T, Gallo M, Messina E, Venneri MA, et al. Pancreatic neuroendocrine neoplasms: Does sex matter? Trends Endocrinol Metab. 2020;31(9):631–41.
pubmed: 32223919 doi: 10.1016/j.tem.2020.02.010
Fanciulli G, Ruggeri RM, Grossrubatscher E, Calzo FL, Wood TD, Faggiano A, et al. Serotonin pathway in carcinoid syndrome: Clinical, diagnostic, prognostic and therapeutic implications. Rev Endocr Metab Disord. 2020;21(4):599–612.
pubmed: 32152781 doi: 10.1007/s11154-020-09547-8
Pandit S, Annamaraju P, Bhusal K. Carcinoid Syndrome. StatPearls. Treasure Island (FL): StatPearls Publishing. Copyright © 2022, StatPearls Publishing LLC.; 2022.
Toth-Fejel S, Pommier RF. Relationships among delay of diagnosis, extent of disease, and survival in patients with abdominal carcinoid tumors. Am J Surg. 2004;187(5):575–9.
pubmed: 15135668 doi: 10.1016/j.amjsurg.2004.01.019
Halperin DM, Shen C, Dasari A, Xu Y, Chu Y, Zhou S, et al. Frequency of carcinoid syndrome at neuroendocrine tumour diagnosis: a population-based study. Lancet Oncol. 2017;18(4):525–34.
pubmed: 28238592 pmcid: 6066284 doi: 10.1016/S1470-2045(17)30110-9
Kimbrough CW, Beal EW, Dillhoff ME, Schmidt CR, Pawlik TM, Lopez-Aguiar AG, et al. Influence of carcinoid syndrome on the clinical characteristics and outcomes of patients with gastroenteropancreatic neuroendocrine tumors undergoing operative resection. Surgery. 2019;165(3):657–63.
pubmed: 30377003 doi: 10.1016/j.surg.2018.09.008
Cai B, Broder MS, Chang E, Yan T, Metz DC. Predictive factors associated with carcinoid syndrome in patients with gastrointestinal neuroendocrine tumors. World J Gastroenterol. 2017;23(40):7283–91.
pubmed: 29142475 pmcid: 5677203 doi: 10.3748/wjg.v23.i40.7283
Gallo M, Muscogiuri G, Pizza G, Ruggeri RM, Barrea L, Faggiano A, et al. The management of neuroendocrine tumours: a nutritional viewpoint. Crit Rev Food Sci Nutr. 2019;59(7):1046–57.
pubmed: 29020456 doi: 10.1080/10408398.2017.1390729
Altieri B, Barrea L, Modica R, Muscogiuri G, Savastano S, Colao A, et al. Nutrition and neuroendocrine tumors: an update of the literature. Rev Endocr Metab Disord. 2018;19(2):159–67.
pubmed: 30267297 doi: 10.1007/s11154-018-9466-z
Ortiz J, Artigas F, Gelpí E. Serotonergic status in human blood. Life Sci. 1988;43(12):983–90.
pubmed: 2459577 doi: 10.1016/0024-3205(88)90543-7
Chakraborti B, Verma D, Guhathakurta S, Jaiswal P, Singh AS, Sinha S, et al. Gender-specific effect of 5-HT and 5-HIAA on threshold level of behavioral symptoms and sex-bias in prevalence of autism spectrum disorder. Front Neurosci. 2019;13:1375.
pubmed: 31998058 doi: 10.3389/fnins.2019.01375
Houghton LA, Brown H, Atkinson W, Morris J, Fell C, Whorwell PJ, et al. 5-hydroxytryptamine signalling in irritable bowel syndrome with diarrhoea: effects of gender and menstrual status. Aliment Pharmacol Ther. 2009;30(9):919–29.
pubmed: 19691669 doi: 10.1111/j.1365-2036.2009.04121.x
Pivac N, Mück-Seler D, Mustapić M, Nenadić-Sviglin K, Kozarić-Kovacić D. Platelet serotonin concentration in alcoholic subjects. Life Sci. 2004;76(5):521–31.
pubmed: 15556165 doi: 10.1016/j.lfs.2004.06.024
van Rumund A, Pavelka L, Esselink RAJ, Geurtz BPM, Wevers RA, Mollenhauer B, et al. Peripheral decarboxylase inhibitors paradoxically induce aromatic L-amino acid decarboxylase. NPJ Parkinsons Dis. 2021;7(1):29.
pubmed: 33741988 pmcid: 7979935 doi: 10.1038/s41531-021-00172-z
Hildebrandt T, Alfano L, Tricamo M, Pfaff DW. Conceptualizing the role of estrogens and serotonin in the development and maintenance of bulimia nervosa. Clin Psychol Rev. 2010;30(6):655–68.
pubmed: 20554102 pmcid: 2910148 doi: 10.1016/j.cpr.2010.04.011
Thibeault AAH, Sanderson JT, Vaillancourt C. Serotonin-estrogen interactions: What can we learn from pregnancy? Biochimie. 2019;161:88–108.
doi: 10.1016/j.biochi.2019.03.023
Thangam EB, Jemima EA, Singh H, Baig MS, Khan M, Mathias CB, et al. The role of histamine and histamine receptors in mast cell-mediated allergy and inflammation: the hunt for new therapeutic targets. Front Immunol. 2018;9:1873.
pubmed: 30150993 pmcid: 6099187 doi: 10.3389/fimmu.2018.01873
Li JN, Li XL, He J, Wang JX, Zhao M, Liang XB, et al. Sex- and afferent-specific differences in histamine receptor expression in vagal afferents of rats: a potential mechanism for sexual dimorphism in prevalence and severity of asthma. Neuroscience. 2015;303:166–77.
pubmed: 26141840 doi: 10.1016/j.neuroscience.2015.06.049
Mackey E, Ayyadurai S, Pohl CS, D’Costa S, Li Y, Moeser AJ. Sexual dimorphism in the mast cell transcriptome and the pathophysiological responses to immunological and psychological stress. Biol Sex Differ. 2016;7:60.
Ridolo E, Incorvaia C, Martignago I, Caminati M, Canonica GW, Senna G. Sex in respiratory and skin allergies. Clin Rev Allergy Immunol. 2019;56(3):322–32.
pubmed: 29306980 doi: 10.1007/s12016-017-8661-0
Comas-Basté O, Sánchez-Pérez S, Veciana-Nogués MT, Latorre-Moratalla M, Vidal-Carou MDC. Histamine intolerance: the current state of the art. Biomolecules. 2020;10(8).
García-Martín E, Ayuso P, Martínez C, Agúndez JA. Improved analytical sensitivity reveals the occurrence of gender-related variability in diamine oxidase enzyme activity in healthy individuals. Clin Biochem. 2007;40(16–17):1339–41.
pubmed: 17826755 doi: 10.1016/j.clinbiochem.2007.07.019
Izquierdo-Casas J, Comas-Basté O, Latorre-Moratalla ML, Lorente-Gascón M, Duelo A, Vidal-Carou MC, et al. Low serum diamine oxidase (DAO) activity levels in patients with migraine. J Physiol Biochem. 2018;74(1):93–9.
pubmed: 28624934 doi: 10.1007/s13105-017-0571-3
Klocker J, Perkmann R, Klein-Weigel P, Mörsdorf G, Drasche A, Klingler A, et al. Continuous administration of heparin in patients with deep vein thrombosis can increase plasma levels of diamine oxidase. Vascul Pharmacol. 2004;40(6):293–300.
pubmed: 15063833 doi: 10.1016/j.vph.2004.02.002
Hamada Y, Shinohara Y, Yano M, Yamamoto M, Yoshio M, Satake K, et al. Effect of the menstrual cycle on serum diamine oxidase levels in healthy women. Clin Biochem. 2013;46(1–2):99–102.
pubmed: 23099198 doi: 10.1016/j.clinbiochem.2012.10.013
Mancuso K, Kaye AD, Boudreaux JP, Fox CJ, Lang P, Kalarickal PL, et al. Carcinoid syndrome and perioperative anesthetic considerations. J Clin Anesth. 2011;23(4):329–41.
pubmed: 21663822 doi: 10.1016/j.jclinane.2010.12.009
Kashuba E, Bailey J, Allsup D, Cawkwell L. The kinin-kallikrein system: physiological roles, pathophysiology and its relationship to cancer biomarkers. Biomarkers. 2013;18(4):279–96.
pubmed: 23672534 doi: 10.3109/1354750X.2013.787544
Sato A, Miura H, Liu Y, Somberg LB, Otterson MF, Demeure MJ, et al. Effect of gender on endothelium-dependent dilation to bradykinin in human adipose microvessels. Am J Physiol Heart Circ Physiol. 2002;283(3):H845–52.
pubmed: 12181110 doi: 10.1152/ajpheart.00160.2002
Hoetzer GL, Stauffer BL, Irmiger HM, Ng M, Smith DT, DeSouza CA. Acute and chronic effects of oestrogen on endothelial tissue-type plasminogen activator release in postmenopausal women. J Physiol. 2003;551(Pt 2):721–8.
pubmed: 12815179 pmcid: 2343226 doi: 10.1113/jphysiol.2003.044107
Modlin IM, Shapiro MD, Kidd M. Carcinoid tumors and fibrosis: an association with no explanation. Am J Gastroenterol. 2004;99(12):2466–78.
pubmed: 15571597 doi: 10.1111/j.1572-0241.2004.40507.x
Blažević A, Zandee WT, Franssen GJH, Hofland J, van Velthuysen MF, Hofland LJ, et al. Mesenteric fibrosis and palliative surgery in small intestinal neuroendocrine tumours. Endocr Relat Cancer. 2018;25(3):245–54.
pubmed: 29255095 doi: 10.1530/ERC-17-0282
Boutzios G, Kaltsas G. Clinical syndromes related to gastrointestinal neuroendocrine neoplasms. Front Horm Res. 2015;44:40–57.
pubmed: 26303703 doi: 10.1159/000382053
The global, regional, and national burden of inflammatory bowel disease in 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol. 2020;5(1):17–30.
Imaeda H, Hibi T. The burden of diverticular disease and its complications: West versus east. Inflamm Intest Dis. 2018;3(2):61–8.
pubmed: 30733949 pmcid: 6361582 doi: 10.1159/000492178
Lapides RA, Savaiano DA. Gender, age, race and lactose intolerance: is there evidence to support a differential symptom response? A scoping review. Nutrients. 2018;10(12).
Porter CK, Gormley R, Tribble DR, Cash BD, Riddle MS. The Incidence and gastrointestinal infectious risk of functional gastrointestinal disorders in a healthy US adult population. Am J Gastroenterol. 2011;106(1):130–8.
pubmed: 20859264 doi: 10.1038/ajg.2010.371
Singh P, Arora A, Strand TA, Leffler DA, Catassi C, Green PH, et al. Global prevalence of celiac disease: Systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2018;16(6):823-36.e2.
pubmed: 29551598 doi: 10.1016/j.cgh.2017.06.037
Spiller R, Aziz Q, Creed F, Emmanuel A, Houghton L, Hungin P, et al. Guidelines on the irritable bowel syndrome: Mechanisms and practical management. Gut. 2007;56(12):1770–98.
pubmed: 17488783 pmcid: 2095723 doi: 10.1136/gut.2007.119446
Tam CC, Rodrigues LC, Viviani L, Dodds JP, Evans MR, Hunter PR, et al. Longitudinal study of infectious intestinal disease in the UK (IID2 study): Incidence in the community and presenting to general practice. Gut. 2012;61(1):69–77.
pubmed: 21708822 doi: 10.1136/gut.2011.238386
Valente S, Di Girolamo G, Forlani M, Biondini A, Scudellari P, De Ronchi D, et al. Sex-specific issues in eating disorders: a clinical and psychopathological investigation. Eat Weight Disord. 2017;22(4):707–15.
pubmed: 28853004 doi: 10.1007/s40519-017-0432-7
Ghaferi AA, Chojnacki KA, Long WD, Cameron JL, Yeo CJ. Pancreatic VIPomas: Subject review and one institutional experience. J Gastrointest Surg. 2008;12(2):382–93.
pubmed: 17510774 doi: 10.1007/s11605-007-0177-0
Hamidi O, Young WF Jr, Iñiguez-Ariza NM, Kittah NE, Gruber L, Bancos C, et al. Malignant pheochromocytoma and paraganglioma: 272 patients over 55 years. J Clin Endocrinol Metab. 2017;102(9):3296–305.
pubmed: 28605453 pmcid: 5587061 doi: 10.1210/jc.2017-00992
Neumann HPH, Tsoy U, Bancos I, Amodru V, Walz MK, Tirosh A, et al. Comparison of pheochromocytoma-specific morbidity and mortality among adults with bilateral pheochromocytomas undergoing total adrenalectomy vs cortical-sparing adrenalectomy. JAMA Netw Open. 2019;2(8):e198898.
Huguet I, Grossman A. Management of endocrine disease: Flushing: current concepts. Eur J Endocrinol. 2017;177(5):R219–29.
pubmed: 28982960 doi: 10.1530/EJE-17-0295
Valassi E, Santos A, Yaneva M, Tóth M, Strasburger CJ, Chanson P, et al. The European Registry on Cushing's syndrome: 2-year experience. Baseline demographic and clinical characteristics. Eur J Endocrinol. 2011;165(3):383–92.
Kitahara CM, Sosa JA. The changing incidence of thyroid cancer. Nat Rev Endocrinol. 2016;12(11):646–53.
pubmed: 27418023 doi: 10.1038/nrendo.2016.110
Soga J, Yakuwa Y, Osaka M. Carcinoid syndrome: a statistical evaluation of 748 reported cases. J Exp Clin Cancer Res. 1999;18(2):133–41.
pubmed: 10464698
Huankang Z, Kuanlin X, Xiaolin H, Witt D. Comparison between tracheal foreign body and bronchial foreign body: a review of 1,007 cases. Int J Pediatr Otorhinolaryngol. 2012;76(12):1719–25.
pubmed: 22944360 doi: 10.1016/j.ijporl.2012.08.008
Lee S, Hess EP, Lohse C, Gilani W, Chamberlain AM, Campbell RL. Trends, characteristics, and incidence of anaphylaxis in 2001–2010: a population-based study. J Allergy Clin Immunol. 2017;139(1):182-8.e2.
pubmed: 27378753 doi: 10.1016/j.jaci.2016.04.029
Lim KH, Tefferi A, Lasho TL, Finke C, Patnaik M, Butterfield JH, et al. Systemic mastocytosis in 342 consecutive adults: Survival studies and prognostic factors. Blood. 2009;113(23):5727–36.
pubmed: 19363219 doi: 10.1182/blood-2009-02-205237
Shah R, Newcomb DC. Sex bias in asthma prevalence and pathogenesis. Front Immunol. 2018;9:2997.
pubmed: 30619350 pmcid: 6305471 doi: 10.3389/fimmu.2018.02997
Beaumont JL, Cella D, Phan AT, Choi S, Liu Z, Yao JC. Comparison of health-related quality of life in patients with neuroendocrine tumors with quality of life in the general US population. Pancreas. 2012;41(3):461–6.
pubmed: 22422138 doi: 10.1097/MPA.0b013e3182328045
Fröjd C, Larsson G, Lampic C, von Essen L. Health related quality of life and psychosocial function among patients with carcinoid tumours. A longitudinal, prospective, and comparative study. Health Qual Life Outcomes. 2007;5:18.
Haugland T, DeVon HA. Symptoms, psychosocial factors, and health-related quality of life in patients with neuroendocrine tumors: an integrative review. Cancer Nurs. 2019;42(4):E36-e46.
pubmed: 29846192 doi: 10.1097/NCC.0000000000000614
Pearman TP, Beaumont JL, Cella D, Neary MP, Yao J. Health-related quality of life in patients with neuroendocrine tumors: an investigation of treatment type, disease status, and symptom burden. Support Care Cancer. 2016;24(9):3695–703.
pubmed: 27029477 doi: 10.1007/s00520-016-3189-z
Jiménez-Fonseca P, Carmona-Bayonas A, Martín-Pérez E, Crespo G, Serrano R, Llanos M, et al. Health-related quality of life in well-differentiated metastatic gastroenteropancreatic neuroendocrine tumors. Cancer Metastasis Rev. 2015;34(3):381–400.
pubmed: 26245646 doi: 10.1007/s10555-015-9573-1
Jacobsen MB, Hanssen LE. Clinical effects of octreotide compared to placebo in patients with gastrointestinal neuroendocrine tumours. Report on a double-blind, randomized trial. J Intern Med. 1995;237(3):269–75.
Halperin DM, Huynh L, Beaumont JL, Cai B, Bhak RH, Narkhede S, et al. Assessment of change in quality of life, carcinoid syndrome symptoms and healthcare resource utilization in patients with carcinoid syndrome. BMC Cancer. 2019;19(1):274.
pubmed: 30922252 pmcid: 6437890 doi: 10.1186/s12885-019-5459-x
Chan DL, Segelov E, Singh S. Everolimus in the management of metastatic neuroendocrine tumours. Therap Adv Gastroenterol. 2017;10(1):132–41.
pubmed: 28286565 doi: 10.1177/1756283X16674660
Martini C, Gamper EM, Wintner L, Nilica B, Sperner-Unterweger B, Holzner B, et al. Systematic review reveals lack of quality in reporting health-related quality of life in patients with gastroenteropancreatic neuroendocrine tumours. Health Qual Life Outcomes. 2016;14(1):127.
pubmed: 27614762 pmcid: 5018190 doi: 10.1186/s12955-016-0527-2
Scandurra C, Modica R, Maldonato NM, Dolce P, Dipietrangelo GG, Centello R, et al. Quality of life in patients with neuroendocrine neoplasms: the role of severity, clinical heterogeneity, and resilience. J Clin Endocrinol Metab. 2021;106(1):e316–27.
pubmed: 33084861 doi: 10.1210/clinem/dgaa760
Bober SL, Varela VS. Sexuality in adult cancer survivors: Challenges and intervention. J Clin Oncol. 2012;30(30):3712–9.
pubmed: 23008322 doi: 10.1200/JCO.2012.41.7915
Feldman JM, Plonk JW. Pituitary-gonadal function in the carcinoid syndrome: Effect of parachlorophynylalanine therapy. Horm Metab Res. 1977;9(2):156–60.
pubmed: 140843 doi: 10.1055/s-0028-1093567
Pfaus JG. Pathways of sexual desire. J Sex Med. 2009;6(6):1506–33.
pubmed: 19453889 doi: 10.1111/j.1743-6109.2009.01309.x
Kato A, Sakuma Y. Neuronal activity in female rat preoptic area associated with sexually motivated behavior. Brain Res. 2000;862(1–2):90–102.
pubmed: 10799673 doi: 10.1016/S0006-8993(00)02076-X
Hull EM, Muschamp JW, Sato S. Dopamine and serotonin: Influences on male sexual behavior. Physiol Behav. 2004;83(2):291–307.
pubmed: 15488546 doi: 10.1016/j.physbeh.2004.08.018
Bancila M, Vergé D, Rampin O, Backstrom JR, Sanders-Bush E, McKenna KE, et al. 5-Hydroxytryptamine2C receptors on spinal neurons controlling penile erection in the rat. Neuroscience. 1999;92(4):1523–37.
pubmed: 10426504 doi: 10.1016/S0306-4522(99)00082-2
Snoeren EM, Veening JG, Olivier B, Oosting RS. Serotonin 1A receptors and sexual behavior in female rats: a review. Pharmacol Biochem Behav. 2014;121:43–52.
pubmed: 24275184 doi: 10.1016/j.pbb.2013.11.017
Hannon J, Hoyer D. Molecular biology of 5-HT receptors. Behav Brain Res. 2008;195(1):198–213.
pubmed: 18571247 doi: 10.1016/j.bbr.2008.03.020
Pavel M, O’Toole D, Costa F, Capdevila J, Gross D, Kianmanesh R, et al. ENETS consensus guidelines update for the management of distant metastatic disease of intestinal, pancreatic, bronchial neuroendocrine neoplasms (NEN) and NEN of unknown primary site. Neuroendocrinology. 2016;103(2):172–85.
pubmed: 26731013 doi: 10.1159/000443167
Strosberg JR, Halfdanarson TR, Bellizzi AM, Chan JA, Dillon JS, Heaney AP, et al. The North American neuroendocrine tumor society consensus guidelines for surveillance and medical management of midgut neuroendocrine tumors. Pancreas. 2017;46(6):707–14.
pubmed: 28609356 pmcid: 5642985 doi: 10.1097/MPA.0000000000000850
Riechelmann RP, Pereira AA, Rego JF, Costa FP. Refractory carcinoid syndrome: a review of treatment options. Ther Adv Med Oncol. 2017;9(2):127–37.
pubmed: 28203303 doi: 10.1177/1758834016675803
Anthony L, Vinik AI. Evaluating the characteristics and the management of patients with neuroendocrine tumors receiving octreotide LAR during a 6-year period. Pancreas. 2011;40(7):987–94.
pubmed: 21697761 doi: 10.1097/MPA.0b013e31821f66b4
Bajetta E, Procopio G, Catena L, Martinetti A, De Dosso S, Ricci S, et al. Lanreotide autogel every 6 weeks compared with Lanreotide microparticles every 3 weeks in patients with well differentiated neuroendocrine tumors: a Phase III Study. Cancer. 2006;107(10):2474–81.
pubmed: 17054107 doi: 10.1002/cncr.22272
di Bartolomeo M, Bajetta E, Buzzoni R, Mariani L, Carnaghi C, Somma L, et al. Clinical efficacy of octreotide in the treatment of metastatic neuroendocrine tumors. A study by the Italian Trials in Medical Oncology Group. Cancer. 1996;77(2):402–8.
Ducreux M, Ruszniewski P, Chayvialle JA, Blumberg J, Cloarec D, Michel H, et al. The antitumoral effect of the long-acting somatostatin analog lanreotide in neuroendocrine tumors. Am J Gastroenterol. 2000;95(11):3276–81.
pubmed: 11095353 doi: 10.1111/j.1572-0241.2000.03210.x
Fisher GA Jr, Wolin EM, Liyanage N, Pitman Lowenthal S, Mirakhur B, Pommier RF, et al. Patient-reported symptom control of diarrhea and flushing in patients with neuroendocrine tumors treated with lanreotide depot/autogel: Results from a randomized, placebo-controlled, double-blind and 32-week open-label study. Oncologist. 2018;23(1):16–24.
pubmed: 29038234 doi: 10.1634/theoncologist.2017-0284
Garland J, Buscombe JR, Bouvier C, Bouloux P, Chapman MH, Chow AC, et al. Sandostatin LAR (long-acting octreotide acetate) for malignant carcinoid syndrome: a 3-year experience. Aliment Pharmacol Ther. 2003;17(3):437–44.
pubmed: 12562458 doi: 10.1046/j.1365-2036.2003.01420.x
Janson ET, Oberg K. Long-term management of the carcinoid syndrome. Treatment with octreotide alone and in combination with alpha-interferon. Acta Oncol. 1993;32(2):225–9.
Khan MS, El-Khouly F, Davies P, Toumpanakis C, Caplin ME. Long-term results of treatment of malignant carcinoid syndrome with prolonged release Lanreotide (Somatuline Autogel). Aliment Pharmacol Ther. 2011;34(2):235–42.
pubmed: 21585408 doi: 10.1111/j.1365-2036.2011.04693.x
Kvols LK, Moertel CG, O'Connell MJ, Schutt AJ, Rubin J, Hahn RG. Treatment of the malignant carcinoid syndrome. Evaluation of a long-acting somatostatin analogue. N Engl J Med. 1986;315(11):663–6.
Martín-Richard M, Massutí B, Pineda E, Alonso V, Marmol M, Castellano D, et al. Antiproliferative effects of lanreotide autogel in patients with progressive, well-differentiated neuroendocrine tumours: a Spanish, multicentre, open-label, single arm phase II study. BMC Cancer. 2013;13:427.
pubmed: 24053191 pmcid: 3853091 doi: 10.1186/1471-2407-13-427
Rubin J, Ajani J, Schirmer W, Venook AP, Bukowski R, Pommier R, et al. Octreotide acetate long-acting formulation versus open-label subcutaneous octreotide acetate in malignant carcinoid syndrome. J Clin Oncol. 1999;17(2):600–6.
pubmed: 10080605 doi: 10.1200/JCO.1999.17.2.600
Ruszniewski P, Ish-Shalom S, Wymenga M, O’Toole D, Arnold R, Tomassetti P, et al. Rapid and sustained relief from the symptoms of carcinoid syndrome: Results from an open 6-month study of the 28-day prolonged-release formulation of lanreotide. Neuroendocrinology. 2004;80(4):244–51.
pubmed: 15627802 doi: 10.1159/000082875
Ruszniewski P, Valle JW, Lombard-Bohas C, Cuthbertson DJ, Perros P, Holubec L, et al. Patient-reported outcomes with lanreotide Autogel/Depot for carcinoid syndrome: an international observational study. Dig Liver Dis. 2016;48(5):552–8.
pubmed: 26917486 doi: 10.1016/j.dld.2015.12.013
Vinik AI, Wolin EM, Liyanage N, Gomez-Panzani E, Fisher GA. Evaluation of lanreotide depot/autogel efficacy and safety as a carcinoid syndrome treatment (elect): a randomized, double-blind, placebo-controlled trial. Endocr Pract. 2016;22(9):1068–80.
pubmed: 27214300 doi: 10.4158/EP151172.OR
Wymenga AN, Eriksson B, Salmela PI, Jacobsen MB, Van Cutsem EJ, Fiasse RH, et al. Efficacy and safety of prolonged-release lanreotide in patients with gastrointestinal neuroendocrine tumors and hormone-related symptoms. J Clin Oncol. 1999;17(4):1111.
pubmed: 10561168 doi: 10.1200/JCO.1999.17.4.1111
Oberg K, Norheim I, Theodorsson E. Treatment of malignant midgut carcinoid tumours with a long-acting somatostatin analogue octreotide. Acta Oncol. 1991;30(4):503–7.
pubmed: 1854508 doi: 10.3109/02841869109092409
Fisher GA Jr, Wolin EM, Liyanage N, Lowenthal SP, Mirakhur B, Pommier RF, et al. Lanreotide therapy in carcinoid syndrome: prospective analysis of patient-reported symptoms in patients responsive to prior octreotide therapy and patients naïve to somatostatin analogue therapy in the elect phase 3 study. Endocr Pract. 2018;24(3):243–55.
pubmed: 29547049 doi: 10.4158/EP172000.OR
Carrasco CH, Charnsangavej C, Ajani J, Samaan NA, Richli W, Wallace S. The carcinoid syndrome: palliation by hepatic artery embolization. AJR Am J Roentgenol. 1986;147(1):149–54.
pubmed: 2424291 doi: 10.2214/ajr.147.1.149
Roche A, Girish BV, de Baère T, Baudin E, Boige V, Elias D, et al. Trans-catheter arterial chemoembolization as first-line treatment for hepatic metastases from endocrine tumors. Eur Radiol. 2003;13(1):136–40.
pubmed: 12541121 doi: 10.1007/s00330-002-1558-0
Kulke MH, Hörsch D, Caplin ME, Anthony LB, Bergsland E, Öberg K, et al. Telotristat ethyl, a tryptophan hydroxylase inhibitor for the treatment of carcinoid syndrome. J Clin Oncol. 2017;35(1):14–23.
pubmed: 27918724 doi: 10.1200/JCO.2016.69.2780
Pavel M, Gross DJ, Benavent M, Perros P, Srirajaskanthan R, Warner RRP, et al. Telotristat ethyl in carcinoid syndrome: Safety and efficacy in the TELECAST phase 3 trial. Endocr Relat Cancer. 2018;25(3):309–22.
pubmed: 29330194 pmcid: 5811631 doi: 10.1530/ERC-17-0455
Cella D, Beaumont JL, Hudgens S, Marteau F, Feuilly M, Houchard A, et al. Relationship between symptoms and health-related quality-of-life benefits in patients with carcinoid syndrome: Post hoc analyses from TELESTAR. Clin Ther. 2018;40(12):2006-20.e2.
pubmed: 30477789 doi: 10.1016/j.clinthera.2018.10.008
Weickert MO, Kaltsas G, Hörsch D, Lapuerta P, Pavel M, Valle JW, et al. Changes in weight associated with telotristat ethyl in the treatment of carcinoid syndrome. Clin Ther. 2018;40(6):952-62.e2.
pubmed: 29724499 doi: 10.1016/j.clinthera.2018.04.006
Hörsch D, Anthony L, Gross DJ, Valle JW, Welin S, Benavent M, et al. Long-term treatment with telotristat ethyl in patients with carcinoid syndrome symptoms: Results from the TELEPATH study. Neuroendocrinology. 2021.
McDermott EW, Guduric B, Brennan MF. Prognostic variables in patients with gastrointestinal carcinoid tumours. Br J Surg. 1994;81(7):1007–9.
pubmed: 7922047 doi: 10.1002/bjs.1800810725
Formica V, Wotherspoon A, Cunningham D, Norman AR, Sirohi B, Oates J, et al. The prognostic role of WHO classification, urinary 5-hydroxyindoleacetic acid and liver function tests in metastatic neuroendocrine carcinomas of the gastroenteropancreatic tract. Br J Cancer. 2007;96(8):1178–82.
pubmed: 17406366 pmcid: 2360161 doi: 10.1038/sj.bjc.6603699
Greenberg RS, Baumgarten DA, Clark WS, Isacson P, McKeen K. Prognostic factors for gastrointestinal and bronchopulmonary carcinoid tumors. Cancer. 1987;60(10):2476–83.
pubmed: 3311348 doi: 10.1002/1097-0142(19871115)60:10<2476::AID-CNCR2820601022>3.0.CO;2-R
Janson ET, Holmberg L, Stridsberg M, Eriksson B, Theodorsson E, Wilander E, et al. Carcinoid tumors: analysis of prognostic factors and survival in 301 patients from a referral center. Ann Oncol. 1997;8(7):685–90.
pubmed: 9296223 doi: 10.1023/A:1008215730767
Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, 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):3063–72.
pubmed: 18565894 doi: 10.1200/JCO.2007.15.4377
Hallet J, Law CH, Cukier M, Saskin R, Liu N, Singh S. Exploring the rising incidence of neuroendocrine tumors: a population-based analysis of epidemiology, metastatic presentation, and outcomes. Cancer. 2015;121(4):589–97.
pubmed: 25312765 doi: 10.1002/cncr.29099
Boyar Cetinkaya R, Aagnes B, Myklebust T, Thiis-Evensen E. Survival in neuroendocrine neoplasms; a report from a large Norwegian population-based study. Int J Cancer. 2018;142(6):1139–47.
pubmed: 29082524 doi: 10.1002/ijc.31137
Rastogi V, Singh D, Mazza JJ, Parajuli D, Yale SH. Flushing disorders associated with gastrointestinal symptoms: Part 1, neuroendocrine tumors, mast cell disorders and hyperbasophila. Clin Med Res. 2018;16(1–2):16–28.
pubmed: 29650525 pmcid: 6108509 doi: 10.3121/cmr.2017.1379a
Modlin IM, Lye KD, Kidd M. A 5-decade analysis of 13,715 carcinoid tumors. Cancer. 2003;97(4):934–59.
pubmed: 12569593 doi: 10.1002/cncr.11105

Auteurs

Rosaria M Ruggeri (RM)

Department of Clinical and Experimental Medicine, Unit of Endocrinology, University of Messina, Messina, Italy. rmruggeri@unime.it.

Barbara Altieri (B)

Division of Endocrinology and Diabetes, Department of Internal Medicine I, University Hospital, University of Würzburg, Würzburg, Germany.

Erika Grossrubatcher (E)

S.C. Endocrinologia, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy.

Roberto Minotta (R)

Department of Clinical Medicine and Surgery, Endocrinology Unit, University Federico II, Naples, Italy.

Maria Grazia Tarsitano (MG)

Department of Experimental Medicine, Sapienza University of Rome, Rome, Italy.

Virginia Zamponi (V)

Endocrinology Unit, Department of Clinical and Molecular Medicine, Sant'Andrea Hospital, Sapienza University of Rome, Rome, Italy.

Andrea MIsidori (A)

Department of Experimental Medicine, Sapienza University of Rome, Rome, Italy.

Antongiulio Faggiano (A)

Endocrinology Unit, Department of Clinical and Molecular Medicine, Sant'Andrea Hospital, Sapienza University of Rome, Rome, Italy.

Anna Maria Colao (AM)

Department of Clinical Medicine and Surgery, Endocrinology Unit, University Federico II, Naples, Italy.
Cattedra Unesco "Educazione Alla Salute E Allo Sviluppo Sostenibile", University Federico II, Naples, Italy.

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