Risk factors for gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs): a three-centric case–control study
Purpose Risk factors for sporadic GEP-NENs are still not well defined. To identify the main clinical risk factors represents the aim of this study performed by three Italian referral centers for NENs. Methods We performed a retrospective case–control study including 148 consecutive sporadic GEP-NENs...
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| Published in | Journal of endocrinological investigation Vol. 45; no. 4; pp. 849 - 857 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Cham
Springer International Publishing
01.04.2022
Springer Nature B.V |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1720-8386 0391-4097 1720-8386 |
| DOI | 10.1007/s40618-021-01715-0 |
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| Abstract | Purpose
Risk factors for sporadic GEP-NENs are still not well defined. To identify the main clinical risk factors represents the aim of this study performed by three Italian referral centers for NENs.
Methods
We performed a retrospective case–control study including 148 consecutive sporadic GEP-NENs and 210 age- and sex-matched controls. We collected data on clinical features, cancer family history and other potential risk factors.
Results
Mean age was 58.3 ± 15.8 years; 50% males, primary site was pancreas (50.7%), followed by ileum (22.3%). The 62.8% and 29.1% of cases were G1 and G2, respectively; the 40% had locally advanced or metastatic disease at diagnosis. Independent risk factors for GEP-NENs were: family history of non-neuroendocrine GEP cancer (OR 2.16, 95% CI 1.31–3.55,
p
= 0.003), type 2 diabetes mellitus (T2DM) (OR 2.5, 95% CI 1.39–4.51,
p
= 0.002) and obesity (OR 1.88, 95% CI 1.18–2.99,
p
= 0.007). In the T2DM subjects, metformin use was a protective factor (OR 0.28, 95% CI 0.08–0.93,
p
= 0.049). T2DM was also associated with a more advanced (OR 2.39, 95% CI 1.05–5.46,
p
= 0.035) and progressive disease (OR 2.47, 95% CI 1.08–5.34,
p
= 0.03). Stratifying cases by primary site, independent risk factors for pancreatic NENs were T2DM (OR 2.57, 95% CI 1.28–5.15,
p
= 0.008) and obesity (OR 1.98, 95% CI 1.11–3.52,
p
= 0.020), while for intestinal NENs family history of non-neuroendocrine GEP cancer (OR 2.46, 95% CI 1.38–4.38,
p
= 0.003) and obesity (OR 1.90, 95% CI 1.08–3.33,
p
= 0.026).
Conclusion
This study reinforces a role for family history of non-neuroendocrine GEP cancer, T2DM and obesity as independent risk factors for GEP-NENs and suggests a role of metformin as a protective factor in T2DM subjects. If confirmed, these findings could have a significant impact on prevention strategies for GEP-NENs. |
|---|---|
| AbstractList | Purpose
Risk factors for sporadic GEP-NENs are still not well defined. To identify the main clinical risk factors represents the aim of this study performed by three Italian referral centers for NENs.
Methods
We performed a retrospective case–control study including 148 consecutive sporadic GEP-NENs and 210 age- and sex-matched controls. We collected data on clinical features, cancer family history and other potential risk factors.
Results
Mean age was 58.3 ± 15.8 years; 50% males, primary site was pancreas (50.7%), followed by ileum (22.3%). The 62.8% and 29.1% of cases were G1 and G2, respectively; the 40% had locally advanced or metastatic disease at diagnosis. Independent risk factors for GEP-NENs were: family history of non-neuroendocrine GEP cancer (OR 2.16, 95% CI 1.31–3.55,
p
= 0.003), type 2 diabetes mellitus (T2DM) (OR 2.5, 95% CI 1.39–4.51,
p
= 0.002) and obesity (OR 1.88, 95% CI 1.18–2.99,
p
= 0.007). In the T2DM subjects, metformin use was a protective factor (OR 0.28, 95% CI 0.08–0.93,
p
= 0.049). T2DM was also associated with a more advanced (OR 2.39, 95% CI 1.05–5.46,
p
= 0.035) and progressive disease (OR 2.47, 95% CI 1.08–5.34,
p
= 0.03). Stratifying cases by primary site, independent risk factors for pancreatic NENs were T2DM (OR 2.57, 95% CI 1.28–5.15,
p
= 0.008) and obesity (OR 1.98, 95% CI 1.11–3.52,
p
= 0.020), while for intestinal NENs family history of non-neuroendocrine GEP cancer (OR 2.46, 95% CI 1.38–4.38,
p
= 0.003) and obesity (OR 1.90, 95% CI 1.08–3.33,
p
= 0.026).
Conclusion
This study reinforces a role for family history of non-neuroendocrine GEP cancer, T2DM and obesity as independent risk factors for GEP-NENs and suggests a role of metformin as a protective factor in T2DM subjects. If confirmed, these findings could have a significant impact on prevention strategies for GEP-NENs. Risk factors for sporadic GEP-NENs are still not well defined. To identify the main clinical risk factors represents the aim of this study performed by three Italian referral centers for NENs. We performed a retrospective case-control study including 148 consecutive sporadic GEP-NENs and 210 age- and sex-matched controls. We collected data on clinical features, cancer family history and other potential risk factors. Mean age was 58.3 ± 15.8 years; 50% males, primary site was pancreas (50.7%), followed by ileum (22.3%). The 62.8% and 29.1% of cases were G1 and G2, respectively; the 40% had locally advanced or metastatic disease at diagnosis. Independent risk factors for GEP-NENs were: family history of non-neuroendocrine GEP cancer (OR 2.16, 95% CI 1.31-3.55, p = 0.003), type 2 diabetes mellitus (T2DM) (OR 2.5, 95% CI 1.39-4.51, p = 0.002) and obesity (OR 1.88, 95% CI 1.18-2.99, p = 0.007). In the T2DM subjects, metformin use was a protective factor (OR 0.28, 95% CI 0.08-0.93, p = 0.049). T2DM was also associated with a more advanced (OR 2.39, 95% CI 1.05-5.46, p = 0.035) and progressive disease (OR 2.47, 95% CI 1.08-5.34, p = 0.03). Stratifying cases by primary site, independent risk factors for pancreatic NENs were T2DM (OR 2.57, 95% CI 1.28-5.15, p = 0.008) and obesity (OR 1.98, 95% CI 1.11-3.52, p = 0.020), while for intestinal NENs family history of non-neuroendocrine GEP cancer (OR 2.46, 95% CI 1.38-4.38, p = 0.003) and obesity (OR 1.90, 95% CI 1.08-3.33, p = 0.026). This study reinforces a role for family history of non-neuroendocrine GEP cancer, T2DM and obesity as independent risk factors for GEP-NENs and suggests a role of metformin as a protective factor in T2DM subjects. If confirmed, these findings could have a significant impact on prevention strategies for GEP-NENs. PurposeRisk factors for sporadic GEP-NENs are still not well defined. To identify the main clinical risk factors represents the aim of this study performed by three Italian referral centers for NENs.MethodsWe performed a retrospective case–control study including 148 consecutive sporadic GEP-NENs and 210 age- and sex-matched controls. We collected data on clinical features, cancer family history and other potential risk factors.ResultsMean age was 58.3 ± 15.8 years; 50% males, primary site was pancreas (50.7%), followed by ileum (22.3%). The 62.8% and 29.1% of cases were G1 and G2, respectively; the 40% had locally advanced or metastatic disease at diagnosis. Independent risk factors for GEP-NENs were: family history of non-neuroendocrine GEP cancer (OR 2.16, 95% CI 1.31–3.55, p = 0.003), type 2 diabetes mellitus (T2DM) (OR 2.5, 95% CI 1.39–4.51, p = 0.002) and obesity (OR 1.88, 95% CI 1.18–2.99, p = 0.007). In the T2DM subjects, metformin use was a protective factor (OR 0.28, 95% CI 0.08–0.93, p = 0.049). T2DM was also associated with a more advanced (OR 2.39, 95% CI 1.05–5.46, p = 0.035) and progressive disease (OR 2.47, 95% CI 1.08–5.34, p = 0.03). Stratifying cases by primary site, independent risk factors for pancreatic NENs were T2DM (OR 2.57, 95% CI 1.28–5.15, p = 0.008) and obesity (OR 1.98, 95% CI 1.11–3.52, p = 0.020), while for intestinal NENs family history of non-neuroendocrine GEP cancer (OR 2.46, 95% CI 1.38–4.38, p = 0.003) and obesity (OR 1.90, 95% CI 1.08–3.33, p = 0.026).ConclusionThis study reinforces a role for family history of non-neuroendocrine GEP cancer, T2DM and obesity as independent risk factors for GEP-NENs and suggests a role of metformin as a protective factor in T2DM subjects. If confirmed, these findings could have a significant impact on prevention strategies for GEP-NENs. Risk factors for sporadic GEP-NENs are still not well defined. To identify the main clinical risk factors represents the aim of this study performed by three Italian referral centers for NENs.PURPOSERisk factors for sporadic GEP-NENs are still not well defined. To identify the main clinical risk factors represents the aim of this study performed by three Italian referral centers for NENs.We performed a retrospective case-control study including 148 consecutive sporadic GEP-NENs and 210 age- and sex-matched controls. We collected data on clinical features, cancer family history and other potential risk factors.METHODSWe performed a retrospective case-control study including 148 consecutive sporadic GEP-NENs and 210 age- and sex-matched controls. We collected data on clinical features, cancer family history and other potential risk factors.Mean age was 58.3 ± 15.8 years; 50% males, primary site was pancreas (50.7%), followed by ileum (22.3%). The 62.8% and 29.1% of cases were G1 and G2, respectively; the 40% had locally advanced or metastatic disease at diagnosis. Independent risk factors for GEP-NENs were: family history of non-neuroendocrine GEP cancer (OR 2.16, 95% CI 1.31-3.55, p = 0.003), type 2 diabetes mellitus (T2DM) (OR 2.5, 95% CI 1.39-4.51, p = 0.002) and obesity (OR 1.88, 95% CI 1.18-2.99, p = 0.007). In the T2DM subjects, metformin use was a protective factor (OR 0.28, 95% CI 0.08-0.93, p = 0.049). T2DM was also associated with a more advanced (OR 2.39, 95% CI 1.05-5.46, p = 0.035) and progressive disease (OR 2.47, 95% CI 1.08-5.34, p = 0.03). Stratifying cases by primary site, independent risk factors for pancreatic NENs were T2DM (OR 2.57, 95% CI 1.28-5.15, p = 0.008) and obesity (OR 1.98, 95% CI 1.11-3.52, p = 0.020), while for intestinal NENs family history of non-neuroendocrine GEP cancer (OR 2.46, 95% CI 1.38-4.38, p = 0.003) and obesity (OR 1.90, 95% CI 1.08-3.33, p = 0.026).RESULTSMean age was 58.3 ± 15.8 years; 50% males, primary site was pancreas (50.7%), followed by ileum (22.3%). The 62.8% and 29.1% of cases were G1 and G2, respectively; the 40% had locally advanced or metastatic disease at diagnosis. Independent risk factors for GEP-NENs were: family history of non-neuroendocrine GEP cancer (OR 2.16, 95% CI 1.31-3.55, p = 0.003), type 2 diabetes mellitus (T2DM) (OR 2.5, 95% CI 1.39-4.51, p = 0.002) and obesity (OR 1.88, 95% CI 1.18-2.99, p = 0.007). In the T2DM subjects, metformin use was a protective factor (OR 0.28, 95% CI 0.08-0.93, p = 0.049). T2DM was also associated with a more advanced (OR 2.39, 95% CI 1.05-5.46, p = 0.035) and progressive disease (OR 2.47, 95% CI 1.08-5.34, p = 0.03). Stratifying cases by primary site, independent risk factors for pancreatic NENs were T2DM (OR 2.57, 95% CI 1.28-5.15, p = 0.008) and obesity (OR 1.98, 95% CI 1.11-3.52, p = 0.020), while for intestinal NENs family history of non-neuroendocrine GEP cancer (OR 2.46, 95% CI 1.38-4.38, p = 0.003) and obesity (OR 1.90, 95% CI 1.08-3.33, p = 0.026).This study reinforces a role for family history of non-neuroendocrine GEP cancer, T2DM and obesity as independent risk factors for GEP-NENs and suggests a role of metformin as a protective factor in T2DM subjects. If confirmed, these findings could have a significant impact on prevention strategies for GEP-NENs.CONCLUSIONThis study reinforces a role for family history of non-neuroendocrine GEP cancer, T2DM and obesity as independent risk factors for GEP-NENs and suggests a role of metformin as a protective factor in T2DM subjects. If confirmed, these findings could have a significant impact on prevention strategies for GEP-NENs. |
| Author | Giannetta, E. Di Meglio, S. Feola, T. Puliani, G. Lenzi, A. Lauretta, R. Colao, A. Appetecchia, M. Isidori, A. M. Cannavale, G. Sesti, F. Modica, R. Minotta, R. Di Vito, V. Faggiano, A. Centello, R. |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35040099$$D View this record in MEDLINE/PubMed |
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| Keywords | Gastroenteropancreatic neuroendocrine neoplasms Obesity Metformin Diabetes mellitus GEP-NET Cancer family history |
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| PublicationTitleAlternate | J Endocrinol Invest |
| PublicationYear | 2022 |
| Publisher | Springer International Publishing Springer Nature B.V |
| Publisher_xml | – name: Springer International Publishing – name: Springer Nature B.V |
| References | HalfdanarsonTRBamletWRMcWilliamsRRHobdayTJBurchPARabeKGRisk factors for pancreatic neuroendocrine tumorsPancreas2014438121912221:CAS:528:DC%2BC2cXhvVWis7rN10.1097/mpa.0000000000000234252915264267883 MuscogiuriGAltieriBAlbertelliMDottoAModicaRBarreaLEpidemiology of pancreatic neuroendocrine neoplasms: a gender perspectiveEndocrine20206924414501:CAS:528:DC%2BB3cXhtVeltLzL10.1007/s12020-020-02331-332468269 RinzivilloMCapursoGCampanaDFazioNPanzutoFSpadaFRisk and protective factors for small intestine neuroendocrine tumors: a prospective case-control studyNeuroendocrinology201610355315371:CAS:528:DC%2BC28Xht1yntL7M10.1159/00044088426356731 GiraldiLVecchioniACarioliGBilottaMLa RosaSImperatoriARisk factors for pancreas and lung neuroendocrine neoplasms: a case–control studyEndocrine20207112332411:CAS:528:DC%2BB3cXhslWgtLrO10.1007/s12020-020-02464-5328691137835148 Lloyd RvoRYKlppelGNRosaiJInternational agency for research on, digestive system tumours2019GenevaWorld Health Organization CapursoGFalconiMPanzutoFRinzivilloMBoninsegnaLBettiniRRisk factors for sporadic pancreatic endocrine tumorsAm J Gastroenterol200910412303430411:CAS:528:DC%2BD1MXhsFShtbfF10.1038/ajg.2009.46619690522 KaerlevLTeglbjaergPSSabroeSKolstadHAAhrensWErikssonMThe importance of smoking and medical history for development of small bowel carcinoid tumor: a European population-based case–control studyCancer Causes Control2002131273410.1023/a:101392222661411899115 BarreaLMuscogiuriGModicaRAltieriBPuglieseGMinottaRCardio-metabolic indices and metabolic syndrome as predictors of clinical severity of gastroenteropancreatic neuroendocrine tumorsFront Endocrinol202110.3389/fendo.2021.649496 HassanMMPhanALiDDagohoyCGLearyCYaoJCFamily history of cancer and associated risk of developing neuroendocrine tumors: a case-control studyCancer Epidemiol Biomark Prev200817495996510.1158/1055-9965.epi-07-0750 HassanMMPhanALiDDagohoyCGLearyCYaoJCRisk factors associated with neuroendocrine tumors: a U.S.-based case-control studyInt J Cancer200812348678731:CAS:528:DC%2BD1cXovFWmurs%3D10.1002/ijc.2352918491401 ZhanH-XCongLZhaoY-PZhangT-PChenGRisk factors for the occurrence of insulinoma: a case-control studyHepatobiliary Pancreat Dis Int201312332432810.1016/s1499-3872(13)60051-x23742779 FraenkelMFaggianoAValkGDEpidemiology of neuroendocrine tumorsNeuroendocrine Tumors20154412310.1159/000381970 Cigrovski BerkovicMCacevTCatela IvkovicTZjacic-RotkvicVKapitanovicSNew insights into the role of chronic inflammation and cytokines in the etiopathogenesis of gastroenteropancreatic neuroendocrine tumorsNeuroendocrinology201499275841:CAS:528:DC%2BC2cXht1WqtrfJ10.1159/00036233924686050 HaugvikS-PHedenströmPKorsæthEValenteRHayesASiukaDDiabetes, smoking, alcohol use, and family history of cancer as risk factors for pancreatic neuroendocrine tumors: a systematic review and meta-analysisNeuroendocrinology201510121331421:CAS:528:DC%2BC2MXovVSltb4%3D10.1159/00037516425613442 AndersenDKKorcMPetersenGMEiblGLiDRickelsMRDiabetes, pancreatogenic diabetes, and pancreatic cancerDiabetes2017665110311101:CAS:528:DC%2BC2sXhtFektLzJ10.2337/db16-1477285072105399609 YuXMaoWZhaiYTongCLiuMMaLAnti-tumor activity of metformin: from metabolic and epigenetic perspectivesOncotarget2016835619562810.18632/oncotarget.136395354934 ValenteRHayesAJHaugvikS-PHedenströmPSiukaDKorsæthERisk and protective factors for the occurrence of sporadic pancreatic endocrine neoplasmsEndocr Relat Cancer20172484054141:CAS:528:DC%2BC1cXitVOjt7jL10.1530/erc-17-004028566532 GodslandIFInsulin resistance and hyperinsulinaemia in the development and progression of cancerClin Sci2009118531533210.1042/cs20090399 BenQZhongJFeiJChenHYvLTanJRisk factors for sporadic pancreatic neuroendocrine tumors: a case-control studySci Rep201610.1038/srep36073277821995080551 WestNEWisePEHerlineAJMuldoonRLChoppWVSchwartzDACarcinoid tumors are 15 times more common in patients with Crohnʼs diseaseInflamm Bowel Dis2007139112911341:STN:280:DC%2BD2svms1Ckug%3D%3D10.1002/ibd.2017217538985 LeonciniECarioliGLa VecchiaCBocciaSRindiGRisk factors for neuroendocrine neoplasms: a systematic review and meta-analysisAnn Oncol201627168811:STN:280:DC%2BC28zjvVSmuw%3D%3D10.1093/annonc/mdv50526487581 ScarpaAChangDKNonesKCorboVPatchA-MBaileyPWhole-genome landscape of pancreatic neuroendocrine tumoursNature2017543764365711:CAS:528:DC%2BC2sXislOmur0%3D10.1038/nature2106328199314 MassironiSCampanaDPuscedduSAlbertelliMFaggianoAPanzutoFSecond primary neoplasms in patients with lung and gastroenteropancreatic neuroendocrine neoplasms: data from a retrospective multi-centric studyDig Liver Dis20215333673741:STN:280:DC%2BB3sjgtFCmtQ%3D%3D10.1016/j.dld.2020.09.03133645508 ChenCCNeugutAIRotterdamHRisk factors for adenocarcinomas and malignant carcinoids of the small intestine: preliminary findingsCancer Epidemiol Biomarkers Prev1994332052071:STN:280:DyaK2c3ptValug%3D%3D8019367 WangZLaiS-TXieLZhaoJ-DMaN-YZhuJMetformin is associated with reduced risk of pancreatic cancer in patients with type 2 diabetes mellitus: a systematic review and meta-analysisDiabetes Res Clin Pract2014106119261:CAS:528:DC%2BC2cXotVaqsb8%3D10.1016/j.diabres.2014.04.00724837144 LagergrenJYeWEkbomAIntestinal cancer after cholecystectomy: is bile involved in carcinogenesis?Gastroenterology200112135425471:STN:280:DC%2BD3MvnvFSntA%3D%3D10.1053/gast.2001.2708311522737 DumanskiJPRasiCBjörklundPDaviesHAliASGrönbergMA MUTYH germline mutation is associated with small intestinal neuroendocrine tumorsEndocr Relat Cancer20172484274431:CAS:528:DC%2BC1cXitVOjt7zI10.1530/erc-17-0196286341805527373 JP Dumanski (1715_CR20) 2017; 24 L Giraldi (1715_CR5) 2020; 71 M Rinzivillo (1715_CR11) 2016; 103 S-P Haugvik (1715_CR16) 2015; 101 DK Andersen (1715_CR22) 2017; 66 RY Lloyd Rvo (1715_CR1) 2019 E Leoncini (1715_CR17) 2016; 27 Q Ben (1715_CR3) 2016 H-X Zhan (1715_CR14) 2013; 12 A Scarpa (1715_CR21) 2017; 543 MM Hassan (1715_CR7) 2008; 17 G Capurso (1715_CR4) 2009; 104 M Cigrovski Berkovic (1715_CR26) 2014; 99 J Lagergren (1715_CR10) 2001; 121 X Yu (1715_CR25) 2016; 8 S Massironi (1715_CR19) 2021; 53 MM Hassan (1715_CR8) 2008; 123 TR Halfdanarson (1715_CR6) 2014; 43 G Muscogiuri (1715_CR27) 2020; 69 L Kaerlev (1715_CR9) 2002; 13 IF Godsland (1715_CR23) 2009; 118 CC Chen (1715_CR15) 1994; 3 Z Wang (1715_CR24) 2014; 106 L Barrea (1715_CR18) 2021 R Valente (1715_CR12) 2017; 24 NE West (1715_CR13) 2007; 13 M Fraenkel (1715_CR2) 2015; 44 |
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VecchiaCBocciaSRindiGRisk factors for neuroendocrine neoplasms: a systematic review and meta-analysisAnn Oncol201627168811:STN:280:DC%2BC28zjvVSmuw%3D%3D10.1093/annonc/mdv50526487581 – reference: GodslandIFInsulin resistance and hyperinsulinaemia in the development and progression of cancerClin Sci2009118531533210.1042/cs20090399 – reference: DumanskiJPRasiCBjörklundPDaviesHAliASGrönbergMA MUTYH germline mutation is associated with small intestinal neuroendocrine tumorsEndocr Relat Cancer20172484274431:CAS:528:DC%2BC1cXitVOjt7zI10.1530/erc-17-0196286341805527373 – reference: RinzivilloMCapursoGCampanaDFazioNPanzutoFSpadaFRisk and protective factors for small intestine neuroendocrine tumors: a prospective case-control studyNeuroendocrinology201610355315371:CAS:528:DC%2BC28Xht1yntL7M10.1159/00044088426356731 – reference: HalfdanarsonTRBamletWRMcWilliamsRRHobdayTJBurchPARabeKGRisk factors for pancreatic neuroendocrine tumorsPancreas2014438121912221:CAS:528:DC%2BC2cXhvVWis7rN10.1097/mpa.0000000000000234252915264267883 – reference: Cigrovski BerkovicMCacevTCatela IvkovicTZjacic-RotkvicVKapitanovicSNew insights into the role of chronic inflammation and cytokines in the etiopathogenesis of gastroenteropancreatic neuroendocrine tumorsNeuroendocrinology201499275841:CAS:528:DC%2BC2cXht1WqtrfJ10.1159/00036233924686050 – reference: WangZLaiS-TXieLZhaoJ-DMaN-YZhuJMetformin is associated with reduced risk of pancreatic cancer in patients with type 2 diabetes mellitus: a systematic review and meta-analysisDiabetes Res Clin Pract2014106119261:CAS:528:DC%2BC2cXotVaqsb8%3D10.1016/j.diabres.2014.04.00724837144 – reference: CapursoGFalconiMPanzutoFRinzivilloMBoninsegnaLBettiniRRisk factors for sporadic pancreatic endocrine tumorsAm J Gastroenterol200910412303430411:CAS:528:DC%2BD1MXhsFShtbfF10.1038/ajg.2009.46619690522 – reference: ScarpaAChangDKNonesKCorboVPatchA-MBaileyPWhole-genome landscape of pancreatic neuroendocrine tumoursNature2017543764365711:CAS:528:DC%2BC2sXislOmur0%3D10.1038/nature2106328199314 – reference: BenQZhongJFeiJChenHYvLTanJRisk factors for sporadic pancreatic neuroendocrine tumors: a case-control studySci Rep201610.1038/srep36073277821995080551 – reference: KaerlevLTeglbjaergPSSabroeSKolstadHAAhrensWErikssonMThe importance of smoking and medical history for development of small bowel carcinoid tumor: a European population-based case–control studyCancer Causes Control2002131273410.1023/a:101392222661411899115 – reference: ZhanH-XCongLZhaoY-PZhangT-PChenGRisk factors for the occurrence of insulinoma: a case-control studyHepatobiliary Pancreat Dis Int201312332432810.1016/s1499-3872(13)60051-x23742779 – reference: GiraldiLVecchioniACarioliGBilottaMLa RosaSImperatoriARisk factors for pancreas and lung neuroendocrine neoplasms: a case–control studyEndocrine20207112332411:CAS:528:DC%2BB3cXhslWgtLrO10.1007/s12020-020-02464-5328691137835148 – reference: BarreaLMuscogiuriGModicaRAltieriBPuglieseGMinottaRCardio-metabolic indices and metabolic syndrome as predictors of clinical severity of gastroenteropancreatic neuroendocrine tumorsFront Endocrinol202110.3389/fendo.2021.649496 – reference: Lloyd RvoRYKlppelGNRosaiJInternational agency for research on, digestive system tumours2019GenevaWorld Health Organization – reference: HassanMMPhanALiDDagohoyCGLearyCYaoJCRisk factors associated with neuroendocrine tumors: a U.S.-based case-control studyInt J Cancer200812348678731:CAS:528:DC%2BD1cXovFWmurs%3D10.1002/ijc.2352918491401 – reference: AndersenDKKorcMPetersenGMEiblGLiDRickelsMRDiabetes, pancreatogenic diabetes, and pancreatic cancerDiabetes2017665110311101:CAS:528:DC%2BC2sXhtFektLzJ10.2337/db16-1477285072105399609 – reference: HaugvikS-PHedenströmPKorsæthEValenteRHayesASiukaDDiabetes, smoking, alcohol use, and family history of cancer as risk factors for pancreatic neuroendocrine tumors: a systematic review and 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Risk factors for sporadic GEP-NENs are still not well defined. To identify the main clinical risk factors represents the aim of this study performed by... Risk factors for sporadic GEP-NENs are still not well defined. To identify the main clinical risk factors represents the aim of this study performed by three... PurposeRisk factors for sporadic GEP-NENs are still not well defined. To identify the main clinical risk factors represents the aim of this study performed by... |
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| SubjectTerms | Adult Aged Cancer Case-Control Studies Chi-Square Distribution Diabetes mellitus (non-insulin dependent) Endocrinology Family medical history Female Humans Ileum Internal Medicine Intestinal Neoplasms - classification Intestinal Neoplasms - epidemiology Intestinal Neoplasms - genetics Italy - epidemiology Male Medical History Taking - statistics & numerical data Medicine Medicine & Public Health Metabolic Diseases Metastases Metformin Middle Aged Neuroendocrine tumors Neuroendocrine Tumors - classification Neuroendocrine Tumors - epidemiology Neuroendocrine Tumors - genetics Obesity Original Article Pancreatic Neoplasms - classification Pancreatic Neoplasms - epidemiology Pancreatic Neoplasms - genetics Prognosis Retrospective Studies Risk Factors Stomach Neoplasms - classification Stomach Neoplasms - epidemiology Stomach Neoplasms - genetics |
| Title | Risk factors for gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs): a three-centric case–control study |
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