Metabolically-healthy Obesity is Associated with Higher Prevalence of Colorectal Adenoma

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2017 Jun 22

PMID 28636624

Citations 5

Authors

Dong Hyun Sinn

Yang Won Min

Hee Jung Son

Poong-Lyul Rhee

Seung Woon Paik

Sung Noh Hong

Geum-Youn Gwak

Affiliations

Soon will be listed here.

Abstract

Background: The risk of colorectal adenoma (CRA), an important precursor of colorectal cancer, is largely unknown among obese individuals without obesity-related metabolic abnormalities, a condition described as metabolically-healthy obese (MHO). The aim of this study was to examine the association among metabolic status, the different categories of body mass index (BMI), and CRA in a large cohort of adults.

Methods: We analyzed the association among metabolic status, BMI categories and CRA in asymptomatic adults who underwent a first-time colonoscopy as part of the comprehensive health check-up program at the Health Promotion Center of Samsung Medical Center, from January 2005 to December 2012. Being metabolically healthy was defined as lacking any metabolic syndrome components and having a homeostasis model assessment of insulin resistance <2.5.

Results: The prevalence of "any," "multiple," and "high-risk" CRA was 25.6%, 8.3%, and 4.4% among 9,182 metabolically-healthy participants, and 35.9%, 12.5%, and 7.0% among 17,407 metabolically-unhealthy participants, respectively. Increased BMI showed a significant dose-dependent relationship with the prevalence of "any," "multiple," and "high-risk" CRA, in both metabolically-healthy and unhealthy participants. In multivariable-adjusted models that accounted for potential confounders including age, sex, smoking, alcohol, first-degree family history of colorectal cancer, and aspirin use, the odds ratio (OR) for any CRA comparing MHO with metabolically-healthy normal-weight (MHNW) participants was 1.25 (95% confidence interval (CI), 1.09-1.43). Further adjustment for metabolic components associated with obesity did not significantly change the association. Similarly, the ORs for multiple CRAs and high risk CRA were higher in MHO participants than MHNW participants [ORs (95% CI), 1.63 (1.31-2.04) and 1.53 (1.14-2.04), respectively].

Conclusions: The MHO phenotype was closely associated with higher prevalence of CRA, including high-risk adenoma. This finding supports the conclusion that MHO increases the risk of colorectal cancer.

Citing Articles

Obesity-Associated Colorectal Cancer.

Gonzalez-Gutierrez L, Motino O, Barriuso D, de la Puente-Aldea J, Alvarez-Frutos L, Kroemer G Int J Mol Sci. 2024; 25(16).

PMID: 39201522 PMC: 11354800. DOI: 10.3390/ijms25168836.

Adenoma to Colorectal Cancer Estimated Transition Rates Stratified by BMI Categories-A Cross-Sectional Analysis of Asymptomatic Individuals from Screening Colonoscopy Program.

Spychalski P, Kobiela J, Wieszczy P, Bugajski M, Regula J, Kaminski M Cancers (Basel). 2022; 14(1).

PMID: 35008224 PMC: 8750540. DOI: 10.3390/cancers14010062.

Metabolically Healthy Obesity Is Associated with an Increased Risk of Colorectal Adenoma Occurrence Diagnosed by Surveillance Colonoscopy.

Chae H, Yang H, Park S, Jung Y, Park J, Park D Gut Liver. 2020; 15(3):383-390.

PMID: 32616681 PMC: 8129661. DOI: 10.5009/gnl20084.

Increased Expression of Resistin in MicroRNA-155-Deficient White Adipose Tissues May Be a Possible Driver of Metabolically Healthy Obesity Transition to Classical Obesity.

Johnson C, Drummer 4th C, Virtue A, Gao T, Wu S, Hernandez M Front Physiol. 2018; 9:1297.

PMID: 30369883 PMC: 6194169. DOI: 10.3389/fphys.2018.01297.

Influence of Obesity and Metabolic Abnormalities on the Risk of Developing Colorectal Neoplasia.

Kim N, Jung Y, Park J, Park D, Sohn C Dig Dis Sci. 2018; 63(11):3126-3133.

PMID: 30094620 DOI: 10.1007/s10620-018-5239-5.

References

Arnlov J, Ingelsson E, Sundstrom J, Lind L . Impact of body mass index and the metabolic syndrome on the risk of cardiovascular disease and death in middle-aged men. Circulation. 2009; 121(2):230-6. DOI: 10.1161/CIRCULATIONAHA.109.887521. View

Fruhbeck G, Toplak H, Woodward E, Halford J, Yumuk V . Need for a paradigm shift in adult overweight and obesity management - an EASO position statement on a pressing public health, clinical and scientific challenge in Europe. Obes Facts. 2014; 7(6):408-16. PMC: 5644793. DOI: 10.1159/000370038. View

Borg B, Gupta N, Zuckerman G, Banerjee B, Gyawali C . Impact of obesity on bowel preparation for colonoscopy. Clin Gastroenterol Hepatol. 2009; 7(6):670-5. PMC: 4151157. DOI: 10.1016/j.cgh.2009.02.014. View

Erarslan E, Turkay C, Koktener A, Koca C, Uz B, Bavbek N . Association of visceral fat accumulation and adiponectin levels with colorectal neoplasia. Dig Dis Sci. 2008; 54(4):862-8. DOI: 10.1007/s10620-008-0440-6. View

Okabayashi K, Ashrafian H, Hasegawa H, Yoo J, Patel V, Harling L . Body mass index category as a risk factor for colorectal adenomas: a systematic review and meta-analysis. Am J Gastroenterol. 2012; 107(8):1175-85. DOI: 10.1038/ajg.2012.180. View

SIMS E . Are there persons who are obese, but metabolically healthy?. Metabolism. 2001; 50(12):1499-504. DOI: 10.1053/meta.2001.27213. View

Soriguer F, Gutierrez-Repiso C, Rubio-Martin E, Garcia-Fuentes E, Almaraz M, Colomo N . Metabolically healthy but obese, a matter of time? Findings from the prospective Pizarra study. J Clin Endocrinol Metab. 2013; 98(6):2318-25. DOI: 10.1210/jc.2012-4253. View

Mutoh M, Teraoka N, Takasu S, Takahashi M, Onuma K, Yamamoto M . Loss of adiponectin promotes intestinal carcinogenesis in Min and wild-type mice. Gastroenterology. 2011; 140(7):2000-8, 2008.e1-2. DOI: 10.1053/j.gastro.2011.02.019. View

Puri R . Is it finally time to dispel the concept of metabolically-healthy obesity?. J Am Coll Cardiol. 2014; 63(24):2687-8. DOI: 10.1016/j.jacc.2014.03.043. View

10.

Poirier P, Giles T, Bray G, Hong Y, Stern J, Pi-Sunyer F . Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss: an update of the 1997 American Heart Association Scientific Statement on Obesity and Heart Disease from the Obesity Committee of the Council on Nutrition,.... Circulation. 2005; 113(6):898-918. DOI: 10.1161/CIRCULATIONAHA.106.171016. View

11.

Bibbins-Domingo K, C Grossman D, Curry S, Davidson K, Epling Jr J, Garcia F . Screening for Colorectal Cancer: US Preventive Services Task Force Recommendation Statement. JAMA. 2016; 315(23):2564-2575. DOI: 10.1001/jama.2016.5989. View

12.

Brochu M, Tchernof A, Dionne I, Sites C, Eltabbakh G, SIMS E . What are the physical characteristics associated with a normal metabolic profile despite a high level of obesity in postmenopausal women?. J Clin Endocrinol Metab. 2001; 86(3):1020-5. DOI: 10.1210/jcem.86.3.7365. View

13.

Chang Y, Jung H, Cho J, Zhang Y, Yun K, Lazo M . Metabolically Healthy Obesity and the Development of Nonalcoholic Fatty Liver Disease. Am J Gastroenterol. 2016; 111(8):1133-40. DOI: 10.1038/ajg.2016.178. View

14.

Chang Y, Ryu S, Suh B, Yun K, Kim C, Cho S . Impact of BMI on the incidence of metabolic abnormalities in metabolically healthy men. Int J Obes (Lond). 2011; 36(9):1187-94. DOI: 10.1038/ijo.2011.247. View

15.

Hamer M, Stamatakis E . Metabolically healthy obesity and risk of all-cause and cardiovascular disease mortality. J Clin Endocrinol Metab. 2012; 97(7):2482-8. PMC: 3387408. DOI: 10.1210/jc.2011-3475. View

16.

Renehan A, Zwahlen M, Minder C, ODwyer S, Shalet S, Egger M . Insulin-like growth factor (IGF)-I, IGF binding protein-3, and cancer risk: systematic review and meta-regression analysis. Lancet. 2004; 363(9418):1346-53. DOI: 10.1016/S0140-6736(04)16044-3. View

17.

Riondino S, Roselli M, Palmirotta R, Della-Morte D, Ferroni P, Guadagni F . Obesity and colorectal cancer: role of adipokines in tumor initiation and progression. World J Gastroenterol. 2014; 20(18):5177-90. PMC: 4017033. DOI: 10.3748/wjg.v20.i18.5177. View

18.

Renehan A, Tyson M, Egger M, Heller R, Zwahlen M . Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet. 2008; 371(9612):569-78. DOI: 10.1016/S0140-6736(08)60269-X. View

19.

Eckel R, Kahn R, Robertson R, Rizza R . Preventing cardiovascular disease and diabetes: a call to action from the American Diabetes Association and the American Heart Association. Circulation. 2006; 113(25):2943-6. DOI: 10.1161/CIRCULATIONAHA.106.176583. View

20.

Endo H, Hosono K, Uchiyama T, Sakai E, Sugiyama M, Takahashi H . Leptin acts as a growth factor for colorectal tumours at stages subsequent to tumour initiation in murine colon carcinogenesis. Gut. 2011; 60(10):1363-71. DOI: 10.1136/gut.2010.235754. View