Abstract
Background
Colorectal cancer incidence is rising in adults < 50 years old, possibly due to obesity. Having bariatric surgery (BRS) should hypothetically reduce this trend, but data are limited. This study compared trends of colorectal cancer (CRC) versus other obesity-related gastrointestinal cancers (OGCs) between morbidly obese and post-BRS subjects.
Material and Methods
This retrospective cohort study investigated OGC resection trends using the 2006–2013 National Inpatient Sample. Patients with prior BRS and non-BRS controls with body mass index ≥ 40 kg/m2 were included (n = 30,279 total). We divided OGCs into CRC and non-CRC OGCs (esophageal, stomach, liver, gallbladder, and pancreas). We calculated OGC resection trends in patients < 50 and ≥ 50 years old using the average annual percent change (AAPC).
Results
BRS patients with OGCs were younger (59.3 vs 62.3 years old), with more female gender (77.4% vs 57.1%) and White race (72.6% vs 67%) compared with controls (p < 0.05). The number of CRC resections increased across all ages in 2006–2013, especially rectal cancer for BRS patients (AAPC + 19.8%, p = 0.04). The steepest rise in early-onset CRC resections was after BRS versus a lesser increase in morbid obesity controls (AAPC + 18.7% and + 13.7%, respectively, p < 0.001). In contrast, non-CRC OGCs increased in our controls but not post-BRS. In a sensitivity analysis, estimated CRC incidence trends also increased post-BRS despite adjusting for increasing BRS prevalence.
Conclusion
Our findings suggest that bariatric surgery is associated with a persistent increase in early-onset CRC trends. Studies are warranted to validate our results and test the impact of bariatric surgery on early-onset CRC biological mechanisms.
Similar content being viewed by others
Abbreviations
- AHRQ:
-
Agency for Healthcare Research and Quality
- AAPC:
-
Average annual percent change
- BRS:
-
Bariatric surgery
- BMI:
-
Body mass index
- CRC:
-
Colorectal cancer
- NIS-HCUP:
-
Nationwide Inpatient Sample-Healthcare Cost and Utilization Project
- NRD:
-
Nationwide Readmission Database
- NHANES:
-
National Health and Nutritional Examination Survey
- OGC:
-
Obesity-Related gastrointestinal cancer
- RYGB:
-
Roux-en-Y gastric bypass surgery
References
Bailey CE, Hu CY, You YN, et al. Increasing disparities in the age-related incidences of colon and rectal cancers in the United States, 1975-2010. JAMA Surg. 2015;150:17–22.
Dwyer AJ, Murphy CC, Boland CR, et al. A summary of the fight colorectal cancer working meeting: exploring risk factors and etiology of sporadic early-age onset colorectal cancer. Gastroenterology. 2019;157:280–8.
Kirzin S, Marisa L, Guimbaud R, et al. Sporadic early-onset colorectal cancer is a specific sub-type of cancer: a morphological, molecular and genetics study. PLoS One. 2014;9:e103159.
Liu PH, Wu K, Ng K, et al. Association of obesity with risk of early-onset colorectal cancer among women. JAMA Oncol. 2019;5:37–44.
Palmer MK, Toth PP. Trends in lipids, obesity, metabolic syndrome, and diabetes mellitus in the United States: an Nhanes analysis (2003–2004 to 2013–2014). 2019;27:309–14.
Asmbs Estimates of Bariatric Surgeries, (Accessed on 02/06/2017).
Lee W-J, Almalki O. Recent advancements in bariatric/metabolic surgery. Ann Gastroenterol Surg. 2017;1:171–9.
Agency for Healthcare Research and Quality. Healthcare cost and utilization project (Hcup): http://www.qualityindicators.ahrq.gov/Downloads/Modules/PSI/V41/TechSpecs/Psi%2015%20accidental%20puncture%20or%20laceration.Pdf, (Last accessed on August 10, 2016).
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;27:1047–55.
Krishna SG, Behzadi J, Hinton A, et al. Effects of bariatric surgery on outcomes of patients with acute pancreatitis. Clin Gastroenterol Hepatol. 2016;14:1001–10.e5.
Lauby-Secretan B, Scoccianti C, Loomis D, et al. Body fatness and Cancer—viewpoint of the Iarc Working Group. N Engl J Med. 2016;375:794–8.
Anderson JE, Chang DC, Talamini MA. A nationwide examination of outcomes of percutaneous cholecystostomy compared with cholecystectomy for acute Cholecystitis, 1998-2010. Surg Endosc. 2013;27:3406–11.
Anderson JE, Hemming AW, Chang DC, et al. Surgical management trends for cholangiocarcinoma in the USA 1998-2009. J Gastrointest Surg. 2012;16:2225–32.
Carroll Jr JE, Hurwitz ZM, Simons JP, et al. In-hospital mortality after resection of biliary tract cancer in the United States. HPB (Oxford). 2010;12:62–7.
Ejaz A, Sachs T, He J, et al. A comparison of open and minimally invasive surgery for hepatic and pancreatic resections using the nationwide inpatient sample. Surgery. 2014;156:538–47.
Hussan H, Gray 2nd DM, Hinton A, et al. Morbid obesity is associated with increased mortality, surgical complications, and incremental health care utilization in the peri-operative period of colorectal cancer surgery. World J Surg. 2016;40:987–94.
Lapar DJ, Stukenborg GJ, Lau CL, et al. Differences in reported esophageal cancer resection outcomes between national clinical and administrative databases. J Thorac Cardiovasc Surg. 2012;144:1152–7.
Mishra A, Otgonsuren M, Venkatesan C, et al. The inpatient economic and mortality impact of hepatocellular carcinoma from 2005 to 2009: analysis of the us Nationwide inpatient sample. Liver Int. 2013;33:1281–6.
Neuwirth MG, Bierema C, Sinnamon AJ, et al. Trends in major upper abdominal surgery for cancer in octogenarians: has there been a change in patient selection? Cancer. 2018;124:125–35.
Sarvepalli S, Garg SK, Sarvepalli SS, et al. Inpatient burden of esophageal cancer and analysis of factors affecting in-hospital mortality and length of stay. Dis Esophagus. 2018:31.
Shi HY, Wang SN, Lee KT. Temporal trends and volume-outcome associations in periampullary cancer patients: a propensity score-adjusted nationwide population-based study. Am J Surg. 2014;207:512–9.
Smith JK, McPhee JT, Hill JS, et al. National outcomes after gastric resection for neoplasm. Arch Surg. 2007;142:387–93.
Solsky I, Friedmann P, Muscarella P, et al. Poor outcomes of gastric cancer surgery after admission through the emergency department. Ann Surg Oncol. 2017;24:1180–7.
Taghizadeh N, Fortin M, Tremblay A. Us hospitalizations for malignant pleural effusions: data from the 2012 National Inpatient Sample. Chest. 2017;151:845–54.
Velez-Serrano JF, Velez-Serrano D, Hernandez-Barrera V, et al. Prediction of in-hospital mortality after pancreatic resection in pancreatic cancer patients: a boosting approach via a population-based study using health administrative data. PLoS One. 2017;12:e0178757.
Wadhwa V, Jobanputra Y, Thota PN, et al. Healthcare utilization and costs associated with Cholangiocarcinoma. Gastroenterol Rep (Oxf). 2017;5:213–8.
Houchens R, Ross D, Elixhauser A. Final report on calculating national inpatient sample (Nis) variances for data years 2012 and later. Hcup Methods Series Report # 2015–09 Online, U.S. Agency for Healthcare Research and Quality, (2015, December 14) http://www.hcup-us.ahrq.gov/reports/methods/methods.jsp.
Ross D Houchens RL, Elixhauser A, Using the Hcup national inpatient sample to estimate trends. 2015. Hcup methods series report # 2006–05 Online., U.S. Agency for Healthcare Research and Quality., (2016, January 4) http://www.hcup-us.ahrq.gov/reports/methods/methods.jsp.
Livingston EH. The incidence of bariatric surgery has plateaued in the U.S. Am J Surg. 2010;200:378–85.
Pope GD, Birkmeyer JD, Finlayson SRG. National trends in utilization and in-hospital outcomes of bariatric surgery. J Gastrointest Surg. 2002;6:855–61.
Cardoso L, Rodrigues D, Gomes L, et al. Short- and long-term mortality after bariatric surgery: a systematic review and meta-analysis. Diabetes Obes Metab. 2017;19:1223–32.
Wee CC, Huskey KW, Bolcic-Jankovic D, et al. Sex, race, and consideration of bariatric surgery among primary care patients with moderate to severe obesity. J Gen Intern Med. 2014;29:68–75.
Lansdorp-Vogelaar I, van Ballegooijen M, Zauber AG, et al. Individualizing colonoscopy screening by sex and race. Gastrointest Endosc. 2009;70:96–108. 08.e1–24
Lieberman DA, Williams JL, Holub JL, et al. Race, ethnicity, and sex affect risk for polyps >9 Mm in average-risk individuals. Gastroenterology. 147(2014):351–8. quiz e14–5
Adams TD, Stroup AM, Gress RE, et al. Cancer incidence and mortality after gastric bypass surgery. Obesity (Silver Spring). 2009;17:796–802.
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;24:1793–9.
Schauer DP, Feigelson HS, Koebnick C, et al. Bariatric surgery and the risk of cancer in a large multisite cohort. Ann Surg. 2019;269:95–101.
Derogar M, Hull MA, Kant P, et al. Increased risk of colorectal cancer after obesity surgery. Ann Surg. 2013;258:983–8.
Mackenzie H, Markar SR. Obesity surgery and risk of cancer. 2018.
Ostlund MP, Lu Y, Lagergren J. Risk of obesity-related cancer after obesity surgery in a population-based cohort study. Ann Surg. 2010;252:972–6.
Tao W, Artama M, von Euler-Chelpin M, Hull M, Ljung R. Colon and rectal cancer risk after bariatric surgery in a multicountry Nordic cohort study. 2019.
Hussan H, Drosdak A, Le Roux M, et al. The long-term impact of Roux-En-Y gastric bypass on colorectal polyp formation and relation to weight loss outcomes. Obes Surg. 2019;
Faria SL, de Oliveira Kelly E, Lins RD, et al. Nutritional management of weight regain after bariatric surgery. Obes Surg. 2010;20:135–9.
Freire RH, Borges MC, Alvarez-Leite JI, et al. Food quality, physical activity, and nutritional follow-up as determinant of weight regain after Roux-en-Y gastric bypass. Nutrition. 2012;28:53–8.
Maleckas A, Gudaitytė R, Petereit R, et al. Weight regain after gastric bypass: etiology and treatment options. Gland Surg. 2016;5:617–24.
Laurino Neto RM, Herbella FAM, Tauil RM, et al. Comorbidities remission after Roux-en-Y gastric bypass for morbid obesity is sustained in a long-term follow-up and correlates with weight regain. Obes Surg. 2012;22:1580–5.
Schlesinger S, Lieb W, Koch M, et al. Body weight gain and risk of colorectal cancer: a systematic review and meta-analysis of observational studies. Obes Rev. 2015;16:607–19.
Sellberg F, Willmer M, Tynelius P, et al. Four years' follow-up changes of physical activity and sedentary time in women undergoing Roux-en-Y gastric bypass surgery and appurtenant children. BMC Surg. 2017;17:133–3.
Sondergaard Nielsen M, Rasmussen S, Just Christensen B, et al. Bariatric surgery does not affect food preferences, but individual changes in food preferences may predict weight loss. 26(2018):1879–87.
Christou NV, Look D, MacLean LD. Weight gain after short- and long-limb gastric bypass in patients followed for longer than 10 years. Ann Surg. 2006;244:734–40.
Karmali S, Brar B, Shi X, et al. Weight recidivism post-bariatric surgery: a systematic review. Obes Surg. 2013;23:1922–33.
Kant P, Sainsbury A, Reed KR, et al. Rectal epithelial cell mitosis and expression of macrophage migration inhibitory factor are increased 3 years after Roux-en-Y gastric bypass (Rygb) for morbid obesity: implications for long-term neoplastic risk following Rygb. Gut. 2011;60:893–901.
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 Biomark Prev. 2008;17:1401–10.
Afshar S, Malcomson F, Kelly SB, et al. Biomarkers of colorectal cancer risk decrease 6 months after Roux-en-Y gastric bypass surgery. Obes Surg. 2018;28:945–54.
Anhe FF, Varin TV, Schertzer JD, et al. The gut microbiota as a mediator of metabolic benefits after bariatric surgery. Can J Diabetes. 2017;41:439–47.
Guo Y, Liu CQ, Shan CX, et al. Gut microbiota after Roux-en-Y gastric bypass and sleeve Gastrectomy in a diabetic rat model: increased diversity and associations of discriminant genera with metabolic Changes. Diabetes Metab Res Rev. 2017;33
Palleja A, Kashani A, Allin KH, et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med. 2016;8:67.
Hussan H, Clinton SK, Roberts K, et al. Fusobacterium's link to colorectal Neoplasia sequenced: a systematic review and future insights. World J Gastroenterol. 2017;23:8626–50.
Li JV, Reshat R, Wu Q, et al. Experimental bariatric surgery in rats generates a cytotoxic chemical environment in the gut contents. Front Microbiol. 2011;2:183.
de Kok TM, van Maanen JM. Evaluation of fecal mutagenicity and colorectal Cancer risk. Mutat Res. 2000;463:53–101.
Hennessy DA, Quan H, Faris PD, et al. Do coder characteristics influence validity of Icd-10 hospital discharge data? BMC Health Serv Res. 2010;10:99.
Quan H, Parsons GA, Ghali WA. Validity of procedure codes in international classification of diseases, 9th revision, clinical modification administrative data. Med Care. 2004;42:801–9.
Golinvaux NS, Bohl DD, Basques BA, et al. Limitations of administrative databases in spine research: a study in obesity. Spine J. 2014;14:2923–8.
Tao W, Konings P, Hull MA, et al. Colorectal Cancer prognosis following obesity surgery in a population-based cohort study. Obes Surg. 2016;
Author information
Authors and Affiliations
Contributions
Dr. Hussan was involved in the conception, design, and interpretation of data and the manuscript’s drafting and critical revision. Mr. Kyle Porter was involved in the study’s design, acquired and statistically analyzed the data, and provided a critical revision of the manuscript. The above authors had full access to all the data in the study and take responsibility for the data’s integrity and the data analysis’ accuracy. Drs. Patel, Akinyeye, Lieberman, and Ahnen were involved in the design, data interpretation, and critical revision of the manuscript. All gave final approval of the submitted manuscript and take responsibility for the integrity of the work.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethical Approval Statement
This article does not contain any studies with human participants or animals performed by any of the authors.
Informed Consent Statement
Informed Consent does not apply to this study.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 257 kb)
Rights and permissions
About this article
Cite this article
Hussan, H., Patel, A., Akinyeye, S. et al. Bariatric Surgery Is Associated with a Recent Temporal Increase in Colorectal Cancer Resections, Most Pronounced in Adults Below 50 Years of Age. OBES SURG 30, 4867–4876 (2020). https://doi.org/10.1007/s11695-020-04902-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11695-020-04902-9