Abstract
Introduction
Obesity is a significant risk factor for cancer incidence and mortality. The number of patients with obesity who undergo bariatric surgery is increasing; however, the impact of such a procedure in affecting the risk of cancer is not completely understood yet.
Methods
We conducted a retrospective unicentric cohort study to characterize the occurrence of cancer in patients who underwent bariatric surgery from January 2010 to December 2018. For cases of cancer identified after bariatric surgery, we performed a cancer-free survival analysis over time. We also performed a cross-sectional analysis of demographic and clinical characteristics at the time of surgery and compared patients with or without a cancer diagnosis.
Results
Of the 2578 patients who underwent bariatric surgery, 117 patients (4.5%) were diagnosed with a cancer. Fifty-nine cases were diagnosed before surgery, and the remaining 58 cases occurred after the bariatric procedure. The prevalence of cancer was more accentuated in women (4.9%) than among men (2.7%). Thyroid and breast cancer were the most frequent before and after bariatric surgery, respectively. On average, patients with cancer diagnosis were older (49.0 vs 43.3 years, p<0.001) and with a lower level of education (7.4 vs 8.6 school years, p=0.002).
Conclusion
Almost all the cases of cancer identified in this study were obesity-related cancers. Further prospective studies are needed to extend the current knowledge regarding the cancer risk profile of patients who undergo bariatric surgery.
Similar content being viewed by others
References
Chooi YC, Ding C, Magkos F. The epidemiology of obesity. Metabolism. 2019;92:6–10. https://doi.org/10.1016/j.metabol.2018.09.005.
Calle EE, Thun MJ. Obesity and cancer. Oncogene. 2004;23(38):6365–78. https://doi.org/10.1038/sj.onc.1207751.
Goodwin PJ, Stambolic V. Impact of the obesity epidemic on cancer. Annu Rev Med. 2015;66:281–96. https://doi.org/10.1146/annurev-med-051613-012328.
Castagneto-Gissey L, Casella-Mariolo J, Casella G, et al. Obesity surgery and cancer: what are the unanswered questions? Front Endocrinol (Lausanne). 2020;11:213. https://doi.org/10.3389/fendo.2020.00213.
Lauby-Secretan B, Scoccianti C, Loomis D, et al. Body fatness and cancer--viewpoint of the IARC Working Group. N Engl J Med. 2016;375(8):794–8. https://doi.org/10.1056/NEJMsr1606602.
Kyrgiou M, Kalliala I, Markozannes G, et al. Adiposity and cancer at major anatomical sites: umbrella review of the literature. BMJ. 2017;356:j477. https://doi.org/10.1136/bmj.j477.
Renehan AG, Tyson M, Egger M, et al. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet. 2008;371(9612):569–78. https://doi.org/10.1016/S0140-6736(08)60269-X.
Zhang K, Luo Y, Dai H, et al. Effects of bariatric surgery on cancer risk: evidence from meta-analysis. Obes Surg. 2020;30(4):1265–72. https://doi.org/10.1007/s11695-019-04368-4.
The Lancet Diabetes E. The obesity-cancer link: of increasing concern. Lancet Diabetes Endocrinol. 2020;8(3):175. https://doi.org/10.1016/S2213-8587(20)30031-0.
World Health Organization. Obesity and Overweight Fact Sheet. [cited January 25, 2021]; Available from: https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight.
Arterburn DE, Telem DA, Kushner RF, et al. Benefits and risks of bariatric surgery in adults: a review. JAMA. 2020;324(9):879–87. https://doi.org/10.1001/jama.2020.12567.
Cheng J, Gao J, Shuai X, et al. The comprehensive summary of surgical versus non-surgical treatment for obesity: a systematic review and meta-analysis of randomized controlled trials. Oncotarget. 2016;7(26):39216–30. https://doi.org/10.18632/oncotarget.9581.
Zhou X, Yu J, Li L, et al. Effects of bariatric surgery on mortality, cardiovascular events, and cancer outcomes in obese patients: systematic review and meta-analysis. Obes Surg. 2016;26(11):2590–601. https://doi.org/10.1007/s11695-016-2144-x.
Wiggins T, Guidozzi N, Welbourn R, et al. Association of bariatric surgery with all-cause mortality and incidence of obesity-related disease at a population level: a systematic review and meta-analysis. PLoS Med. 2020;17(7):e1003206. https://doi.org/10.1371/journal.pmed.1003206.
Sinclair P, Brennan DJ, le Roux CW. Gut adaptation after metabolic surgery and its influences on the brain, liver and cancer. Nat Rev Gastroenterol Hepatol. 2018;15(10):606–24. https://doi.org/10.1038/s41575-018-0057-y.
Colquitt JL, Pickett K, Loveman E, et al. Surgery for weight loss in adults. Cochrane Database Syst Rev. 2014;8:CD003641. https://doi.org/10.1002/14651858.CD003641.pub4.
Carlsson LMS, Sjoholm K, Jacobson P, et al. Life expectancy after bariatric surgery in the Swedish obese subjects study. N Engl J Med. 2020;383(16):1535–43. https://doi.org/10.1056/NEJMoa2002449.
Casagrande DS, Rosa DD, Umpierre D, et al. Incidence of cancer following bariatric surgery: systematic review and meta-analysis. Obes Surg. 2014;24(9):1499–509. Epub 2014/05/13. https://doi.org/10.1007/s11695-014-1276-0.
Schauer DP, Feigelson HS, Koebnick C, et al. Bariatric surgery and the risk of cancer in a large multisite cohort. Ann Surg. 2019;269(1):95–101. https://doi.org/10.1097/SLA.0000000000002525.
Bruno DS, Berger NA. Impact of bariatric surgery on cancer risk reduction. Ann Transl Med. 2020;8(Suppl 1):S13. https://doi.org/10.21037/atm.2019.09.26.
Hassinger TE, Mehaffey JH, Hawkins RB, et al. Overall and estrogen receptor-positive breast cancer incidences are decreased following bariatric surgery. Obes Surg. 2019;29(3):776–81. https://doi.org/10.1007/s11695-018-3598-9.
Tee MC, Cao Y, Warnock GL, et al. Effect of bariatric surgery on oncologic outcomes: a systematic review and meta-analysis. Surg Endosc. 2013;27(12):4449–56. https://doi.org/10.1007/s00464-013-3127-9.
Mackenzie H, Markar SR, Askari A, et al. Obesity surgery and risk of cancer. Br J Surg. 2018;105(12):1650–7. https://doi.org/10.1002/bjs.10914.
Tao W, Konings P, Hull MA, et al. Colorectal cancer prognosis following obesity surgery in a population-based cohort study. Obes Surg. 2017;27(5):1233–9. https://doi.org/10.1007/s11695-016-2431-6.
Aravani A, Downing A, Thomas JD, et al. Obesity surgery and risk of colorectal and other obesity-related cancers: an English population-based cohort study. Cancer Epidemiol. 2018;53:99–104. https://doi.org/10.1016/j.canep.2018.01.002.
Tao W, Artama M, von Euler-Chelpin M, et al. Colon and rectal cancer risk after bariatric surgery in a multicountry Nordic cohort study. Int J Cancer. 2020;147(3):728–35. https://doi.org/10.1002/ijc.32770.
Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9. https://doi.org/10.1007/BF00280883.
Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120(16):1640–5. https://doi.org/10.1161/CIRCULATIONAHA.109.192644.
Adams TD, Stroup AM, Gress RE, et al. Cancer incidence and mortality after gastric bypass surgery. Obesity (Silver Spring). 2009;17(4):796–802. https://doi.org/10.1038/oby.2008.610.
International Agency for Research on Cancer, World Health Organization. The Global Cancer Observatory, Population Fact Sheets – Portugal. [cited February 23, 2021]; Available from: https://gco.iarc.fr/today/data/factsheets/populations/620-portugal-fact-sheets.pdf.
Instituto Português de Oncologia do Porto Francisco Gentil. Registo Oncológico 2017. [cited February 23, 2021]; Available from: https://www.ipoporto.pt/dev/wp-content/uploads/2019/03/Registo-Oncol%C3%B3gico-2017.pdf .
Byrne FL, Martin AR, Kosasih M, Caruana BT, Farrell R. The role of hyperglycemia in endometrial cancer pathogenesis. Cancers (Basel). 2020;12(5). doi: 10.3390/cancers12051191.
Winder AA, Kularatna M, MacCormick AD. Does bariatric surgery affect the incidence of endometrial cancer development? A systematic review. Obes Surg. 2018;28(5):1433–40. https://doi.org/10.1007/s11695-018-3151-x.
Staley SA, Tucker KR, Clark LH. The role of obesity in the development and management of gynecologic cancer. Obstet Gynecol Surv. 2020;75(5):308–16. https://doi.org/10.1097/OGX.0000000000000779.
Rathmell JC. Obesity, immunity, and cancer. N Engl J Med. 2021;384(12):1160–2. https://doi.org/10.1056/NEJMcibr2035081.
Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009;106(7):2365–70. https://doi.org/10.1073/pnas.0812600106.
Rogers CJ, Prabhu KS, Vijay-Kumar M. The microbiome and obesity-an established risk for certain types of cancer. Cancer J. 2014;20(3):176–80. https://doi.org/10.1097/PPO.0000000000000049.
Feigelson HS, Caan B, Weinmann S, et al. Bariatric surgery is associated with reduced risk of breast cancer in both premenopausal and postmenopausal women. Ann Surg. 2020;272(6):1053–9. https://doi.org/10.1097/SLA.0000000000003331.
Anveden A, Taube M, Peltonen M, et al. Long-term incidence of female-specific cancer after bariatric surgery or usual care in the Swedish Obese Subjects Study. Gynecol Oncol. 2017;145(2):224–9. https://doi.org/10.1016/j.ygyno.2017.02.036.
Winder AA, Kularatna M, MacCormick AD. Does bariatric surgery affect the incidence of breast cancer development? A systematic review. Obes Surg. 2017;27(11):3014–20. https://doi.org/10.1007/s11695-017-2901-5.
Hussan H, Stanich PP, Gray 2nd DM, et al. Prior bariatric surgery is linked to improved colorectal cancer surgery outcomes and costs: a propensity-matched analysis. Obes Surg. 2017;27(4):1047–55. https://doi.org/10.1007/s11695-016-2421-8.
Davidson LE, Adams TD. Does bariatric surgery increase or reduce colorectal cancer risk-is the jury still out? JAMA Surg. 2020;55(5):402–3. https://doi.org/10.1001/jamasurg.2020.0090.
Musella M, Berardi G, Bocchetti A, et al. Esophagogastric neoplasms following bariatric surgery: an updated systematic review. Obes Surg. 2019;29(8):2660–9. https://doi.org/10.1007/s11695-019-03951-z.
Orlando G, Pilone V, Vitiello A, et al. Gastric cancer following bariatric surgery: a review. Surg Laparosc Endosc Percutan Tech. 2014;24(5):400–5. https://doi.org/10.1097/SLE.0000000000000050.
Almazeedi S, El-Abd R, Al-Khamis A, et al. Role of bariatric surgery in reducing the risk of colorectal cancer: a meta-analysis. Br J Surg. 2020;107(4):348–54. https://doi.org/10.1002/bjs.11494.
Afshar S, Kelly SB, Seymour K, et al. The effects of bariatric surgery on colorectal cancer risk: systematic review and meta-analysis. Obes Surg. 2014;24(10):1793–9. https://doi.org/10.1007/s11695-014-1359-y.
Sainsbury A, Goodlad RA, Perry SL, et al. Increased colorectal epithelial cell proliferation and crypt fission associated with obesity and roux-en-Y gastric bypass. Cancer Epidemiol Biomarkers Prev. 2008;17(6):1401–10. https://doi.org/10.1158/1055-9965.EPI-07-2874.
Ostlund MP, Lu Y, Lagergren J. Risk of obesity-related cancer after obesity surgery in a population-based cohort study. Ann Surg. 2010;252(6):972–6. https://doi.org/10.1097/SLA.0b013e3181e33778.
Sjostrom L, Gummesson A, Sjostrom CD, et al. Effects of bariatric surgery on cancer incidence in obese patients in Sweden (Swedish Obese Subjects Study): a prospective, controlled intervention trial. Lancet Oncol. 2009;10(7):653–62. https://doi.org/10.1016/S1470-2045(09)70159-7.
Ghiassi S, Morton JM. Safety and efficacy of bariatric and metabolic surgery. Curr Obes Rep. 2020;9(2):159–64. https://doi.org/10.1007/s13679-020-00377-y.
Acknowledgements
We would like to thank the following members of the CRIO Group for their valuable contributions: Ana Varela, André Pinho, Carla Galego, Cidália Gil, Cristina Martins, Diva Melim, Eduardo Lima da Costa, Eduardo Pinto, Eva Lau, Flora Correia, Hugo Sousa, Inês Magalhães, Isabel Brandão, Luís Miguel Pereira, Marco Silva, Patrícia Nunes, Selma Souto, and Sertório Manuel Andrade. We would also like to acknowledge the support of Daniela Salazar, Fernando Mendonça, João Sérgio Neves, Jorge Pedro, Maria João Ferreira, Maria Manuel Silva, Marta Canha, and Vanessa Guerreiro.
Author information
Authors and Affiliations
Consortia
Corresponding author
Ethics declarations
Ethics Approval
For this type of study, formal consent is not required.
Informed Consent
Informed consent does not apply.
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Key Points
•Patients with obesity are at greater risk of having cancer.
•Thyroid and breast cancer were the most frequent before and after bariatric surgery, respectively.
•Cancer risk after bariatric surgery could depend on the procedure undergone, the patient’s gender, and the type of cancer.
•Further studies with long-term follow-up need to be carried out in bariatric populations.
Rights and permissions
About this article
Cite this article
Brito, H., Santos, A.C., Preto, J. et al. Obesity and Cancer: the Profile of a Population who Underwent Bariatric Surgery. OBES SURG 31, 4682–4691 (2021). https://doi.org/10.1007/s11695-021-05626-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11695-021-05626-0