Association of metabolic obesity phenotypes with risk of overall and site-specific cancers: a systematic review and meta-analysis of cohort studies.
Journal
British journal of cancer
ISSN: 1532-1827
Titre abrégé: Br J Cancer
Pays: England
ID NLM: 0370635
Informations de publication
Date de publication:
24 Sep 2024
24 Sep 2024
Historique:
received:
17
10
2023
accepted:
13
09
2024
revised:
05
09
2024
medline:
25
9
2024
pubmed:
25
9
2024
entrez:
24
9
2024
Statut:
aheadofprint
Résumé
Adiposity is a known risk factor for certain cancers; however, it is not clear whether the risk of cancer differs between individuals with high adiposity but different metabolic health status. The aim of this systematic literature review and meta-analysis of cohort studies was to evaluate associations between metabolic obesity phenotypes and overall and site-specific cancer risk. PubMed and Embase databases were used to identify relevant cohort studies up to the 6th of June 2023. Random-effects models were used to estimate summary relative risks (SRRs) and 95% confidence intervals (CIs) for the association between metabolic obesity phenotypes and cancer risk. Certainty of evidence was assessed using the Cochrane methods and the GRADE tool. This study is registered with PROSPERO, number CRD42024549511. A total of 15,556 records were screened, and 31 publications covering 15 unique cohort studies were included in this analysis. Of these studies, 22 were evaluated as being at low risk of bias and 9 at moderate risk of bias. Compared to metabolically healthy normal-weight individuals (MHNW), metabolically unhealthy overweight/obese (MUOW/OB) individuals had a higher risk of overall (SRR = 1.21, 95% CI = 1.02-1.44, n = 3 studies, high certainty) and obesity-related cancers (SRR = 1.42, 95% CI = 1.15-1.74, n = 3, very low certainty). Specifically, MUOW/OB individuals were at higher risk of cancers of the postmenopausal breast (SRR = 1.32, 95% CI = 1.17-1.48, n = 7, low certainty), colorectum (SRR = 1.24, 95% CI = 1.16-1.31, n = 6, moderate certainty), endometrium (SRR = 2.31, 95% CI = 2.08-2.57, n = 4, high certainty), thyroid (SRR = 1.42, 95% CI = 1.29-1.57, n = 4, moderate certainty), kidney (SRR = 1.71, 95% CI = 1.40-2.10, n = 3, low certainty), pancreas (SRR = 1.35, 95% CI = 1.24-1.47, n = 3, high certainty), liver (SRR = 1.81, 95% CI = 1.36-2.42, n = 2, moderate certainty), gallbladder (SRR = 1.42, 95% CI = 1.17-1.73, n = 2, high certainty), bladder (SRR = 1.36, 95% CI = 1.19-1.56, n = 2, moderate certainty), and stomach (SRR = 1.50, 95% CI = 1.12-2.01, n = 2, high certainty). In addition, we found elevated risks of most of these cancers among individuals classified as MUNW and MHOW/OB phenotypes compared to those with MHNW phenotype. Our stratified analyses according to metabolic obesity phenotypes suggested that the elevated risks of some cancers were stronger in individuals with MUOW/OB versus those with MHOW/OB or MUNW phenotypes. These findings suggest that both higher adiposity and metabolic dysfunction were independently associated with increased risk of several cancers, with the strongest associations generally observed among those with both metabolic dysfunction and obesity.
Sections du résumé
BACKGROUND
BACKGROUND
Adiposity is a known risk factor for certain cancers; however, it is not clear whether the risk of cancer differs between individuals with high adiposity but different metabolic health status. The aim of this systematic literature review and meta-analysis of cohort studies was to evaluate associations between metabolic obesity phenotypes and overall and site-specific cancer risk.
METHODS
METHODS
PubMed and Embase databases were used to identify relevant cohort studies up to the 6th of June 2023. Random-effects models were used to estimate summary relative risks (SRRs) and 95% confidence intervals (CIs) for the association between metabolic obesity phenotypes and cancer risk. Certainty of evidence was assessed using the Cochrane methods and the GRADE tool. This study is registered with PROSPERO, number CRD42024549511.
RESULTS
RESULTS
A total of 15,556 records were screened, and 31 publications covering 15 unique cohort studies were included in this analysis. Of these studies, 22 were evaluated as being at low risk of bias and 9 at moderate risk of bias. Compared to metabolically healthy normal-weight individuals (MHNW), metabolically unhealthy overweight/obese (MUOW/OB) individuals had a higher risk of overall (SRR = 1.21, 95% CI = 1.02-1.44, n = 3 studies, high certainty) and obesity-related cancers (SRR = 1.42, 95% CI = 1.15-1.74, n = 3, very low certainty). Specifically, MUOW/OB individuals were at higher risk of cancers of the postmenopausal breast (SRR = 1.32, 95% CI = 1.17-1.48, n = 7, low certainty), colorectum (SRR = 1.24, 95% CI = 1.16-1.31, n = 6, moderate certainty), endometrium (SRR = 2.31, 95% CI = 2.08-2.57, n = 4, high certainty), thyroid (SRR = 1.42, 95% CI = 1.29-1.57, n = 4, moderate certainty), kidney (SRR = 1.71, 95% CI = 1.40-2.10, n = 3, low certainty), pancreas (SRR = 1.35, 95% CI = 1.24-1.47, n = 3, high certainty), liver (SRR = 1.81, 95% CI = 1.36-2.42, n = 2, moderate certainty), gallbladder (SRR = 1.42, 95% CI = 1.17-1.73, n = 2, high certainty), bladder (SRR = 1.36, 95% CI = 1.19-1.56, n = 2, moderate certainty), and stomach (SRR = 1.50, 95% CI = 1.12-2.01, n = 2, high certainty). In addition, we found elevated risks of most of these cancers among individuals classified as MUNW and MHOW/OB phenotypes compared to those with MHNW phenotype. Our stratified analyses according to metabolic obesity phenotypes suggested that the elevated risks of some cancers were stronger in individuals with MUOW/OB versus those with MHOW/OB or MUNW phenotypes.
CONCLUSION
CONCLUSIONS
These findings suggest that both higher adiposity and metabolic dysfunction were independently associated with increased risk of several cancers, with the strongest associations generally observed among those with both metabolic dysfunction and obesity.
Identifiants
pubmed: 39317703
doi: 10.1038/s41416-024-02857-7
pii: 10.1038/s41416-024-02857-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Brown KF, Rumgay H, Dunlop C, Ryan M, Quartly F, Cox A, et al. The fraction of cancer attributable to modifiable risk factors in England, Wales, Scotland, Northern Ireland, and the United Kingdom in 2015. Br J Cancer. 2018;118:1130–41.
pubmed: 29567982
pmcid: 5931106
doi: 10.1038/s41416-018-0029-6
Islami F, Goding Sauer A, Miller KD, Siegel RL, Fedewa SA, Jacobs EJ, et al. Proportion and number of cancer cases and deaths attributable to potentially modifiable risk factors in the United States. CA Cancer J Clin. 2018;68:31–54.
pubmed: 29160902
doi: 10.3322/caac.21440
Soerjomataram I, Shield K, Marant-Micallef C, Vignat J, Hill C, Rogel A, et al. Cancers related to lifestyle and environmental factors in France in 2015. Eur J Cancer. 2018;105:103–13.
pubmed: 30445359
doi: 10.1016/j.ejca.2018.09.009
Pati S, Irfan W, Jameel A, Ahmed S, Shahid RK. Obesity and cancer: a current overview of epidemiology, pathogenesis, outcomes, and management. Cancers. 2023;15:485.
Lauby-Secretan B, Scoccianti C, Loomis D, Grosse Y, Bianchini F, Straif K, et al. Body fatness and cancer—viewpoint of the IARC Working Group. N Engl J Med. 2016;375:794–8.
pubmed: 27557308
pmcid: 6754861
doi: 10.1056/NEJMsr1606602
World Cancer Research Fund and American Institute for Cancer Research. Diet, nutrition, physical activity and cancer: a global perspective. The 2018 Third Expert Report; 2018. Available at https://www.wcrf.org/wp-content/uploads/2021/02/Summary-of-Third-Expert-Report-2018.pdf .
Murphy N, Jenab M, Gunter MJ. Adiposity and gastrointestinal cancers: epidemiology, mechanisms and future directions. Nat Rev Gastroenterol Hepatol. 2018;15:659–70.
pubmed: 29970888
doi: 10.1038/s41575-018-0038-1
Dashti SG, Simpson JA, Viallon V, Karahalios A, Moreno-Betancur M, Brasky T, et al. Adiposity and breast, endometrial, and colorectal cancer risk in postmenopausal women: quantification of the mediating effects of leptin, C-reactive protein, fasting insulin, and estradiol. Cancer Med. 2022;11:1145–59.
pubmed: 35048536
pmcid: 8855919
doi: 10.1002/cam4.4434
Gunter MJ, Hoover DR, Yu H, Wassertheil-Smoller S, Rohan TE, Manson JE, et al. Insulin, insulin-like growth factor-I, and risk of breast cancer in postmenopausal women. J Natl Cancer Inst. 2009;101:48–60.
pubmed: 19116382
pmcid: 2639294
doi: 10.1093/jnci/djn415
Hvidtfeldt UA, Gunter MJ, Lange T, Chlebowski RT, Lane D, Farhat GN, et al. Quantifying mediating effects of endogenous estrogen and insulin in the relation between obesity, alcohol consumption, and breast cancer. Cancer Epidemiol Biomark Prev. 2012;21:1203–12.
doi: 10.1158/1055-9965.EPI-12-0310
Bell JA, Kivimaki M, Hamer M. Metabolically healthy obesity and risk of incident type 2 diabetes: a meta-analysis of prospective cohort studies. Obes Rev. 2014;15:504–15.
pubmed: 24661566
pmcid: 4309497
doi: 10.1111/obr.12157
Hamzeh B, Pasdar Y, Moradi S, Darbandi M, Rahmani N, Shakiba E, et al. Metabolically healthy versus unhealthy obese phenotypes in relation to hypertension incidence; a prospective cohort study. BMC Cardiovasc Disord. 2022;22:106.
pubmed: 35287586
pmcid: 8922873
doi: 10.1186/s12872-022-02553-5
Meng M, Guo Y, Kuang Z, Liu L, Cai Y, Ni X. Risk of stroke among different metabolic obesity phenotypes: a systematic review and meta-analysis. Front Cardiovasc Med. 2022;9:844550.
pubmed: 35548434
pmcid: 9081493
doi: 10.3389/fcvm.2022.844550
Smith GI, Mittendorfer B, Klein S. Metabolically healthy obesity: facts and fantasies. J Clin Invest. 2019;129:3978–89.
pubmed: 31524630
pmcid: 6763224
doi: 10.1172/JCI129186
Chung HS, Lee JS, Song E, Kim JA, Roh E, Yu JH, et al. Effect of metabolic health and obesity phenotype on the risk of pancreatic cancer: a nationwide population-based cohort study. Cancer Epidemiol Biomark Prev. 2021;30:521–8.
doi: 10.1158/1055-9965.EPI-20-1262
Gunter MJ, Xie X, Xue X, Kabat GC, Rohan TE, Wassertheil-Smoller S, et al. Breast cancer risk in metabolically healthy but overweight postmenopausal women. Cancer Res. 2015;75:270–4.
pubmed: 25593034
pmcid: 4657855
doi: 10.1158/0008-5472.CAN-14-2317
Kim JW, Ahn ST, Oh MM, Moon DG, Han K, Park HS. Incidence of prostate cancer according to metabolic health status: a nationwide cohort study. J Korean Med Sci. 2019;34:e49.
pubmed: 30787682
pmcid: 6374548
doi: 10.3346/jkms.2019.34.e49
Kliemann N, Ould Ammar R, Biessy C, Gicquiau A, Katzke V, Kaaks R, et al. Metabolically defined body size phenotypes and risk of endometrial cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC). Cancer Epidemiol Biomark Prev. 2022;31:1359–67.
doi: 10.1158/1055-9965.EPI-22-0160
Mahamat-Saleh Y, Rinaldi S, Kaaks R, Biessy C, Gonzalez-Gil EM, Murphy N, et al. Metabolically defined body size and body shape phenotypes and risk of postmenopausal breast cancer in the European Prospective Investigation into Cancer and Nutrition. Cancer Med. 2023;12:12668–82.
pubmed: 37096432
pmcid: 10278526
doi: 10.1002/cam4.5896
Murphy N, Cross AJ, Abubakar M, Jenab M, Aleksandrova K, Boutron-Ruault MC, et al. A nested case-control study of metabolically defined body size phenotypes and risk of colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC). PLoS Med. 2016;13:e1001988.
pubmed: 27046222
pmcid: 4821615
doi: 10.1371/journal.pmed.1001988
Cao Z, Zheng X, Yang H, Li S, Xu F, Yang X, et al. Association of obesity status and metabolic syndrome with site-specific cancers: a population-based cohort study. Br J Cancer. 2020;123:1336–44.
pubmed: 32728095
pmcid: 7555864
doi: 10.1038/s41416-020-1012-6
Park B, Kim S, Kim H, Cha C, Chung MS. Associations between obesity, metabolic health, and the risk of breast cancer in East Asian women. Br J Cancer. 2021;125:1718–25.
pubmed: 34552203
pmcid: 8651731
doi: 10.1038/s41416-021-01540-5
Kabat GC, Kim MY, Stefanick M, Ho GYF, Lane DS, Odegaard AO, et al. Metabolic obesity phenotypes and risk of colorectal cancer in postmenopausal women. Int J Cancer. 2018;143:543–51.
pubmed: 29488210
pmcid: 6876750
doi: 10.1002/ijc.31345
Moore LL, Chadid S, Singer MR, Kreger BE, Denis GV. Metabolic health reduces risk of obesity-related cancer in Framingham study adults. Cancer Epidemiol Biomark Prev. 2014;23:2057–65.
doi: 10.1158/1055-9965.EPI-14-0240
Lin CJ, Chang YC, Cheng TY, Lo K, Liu SJ, Yeh TL. The association between metabolically healthy obesity and risk of cancer: a systematic review and meta-analysis of prospective cohort studies. Obes Rev. 2020;21:e13049.
pubmed: 32476278
doi: 10.1111/obr.13049
Goodarzi G, Mozaffari H, Raeisi T, Mehravar F, Razi B, Ghazi ML, et al. Metabolic phenotypes and risk of colorectal cancer: a systematic review and meta-analysis of cohort studies. BMC Cancer. 2022;22:89.
pubmed: 35062912
pmcid: 8781040
doi: 10.1186/s12885-021-09149-w
Zheng X, Peng R, Xu H, Lin T, Qiu S, Wei Q, et al. The association between metabolic status and risk of cancer among patients with obesity: metabolically healthy obesity vs. metabolically unhealthy obesity. Front Nutr. 2022;9:783660.
pubmed: 35284439
pmcid: 8914254
doi: 10.3389/fnut.2022.783660
Lee J, Kwak SY, Park D, Kim GE, Park CY, Shin MJ. Prolonged or transition to metabolically unhealthy status, regardless of obesity status, is associated with higher risk of cardiovascular disease incidence and mortality in Koreans. Nutrients. 2022;14:1644.
Moon SG, Park B. The association between metabolic syndrome and colorectal cancer risk by obesity status in Korean women: a nationwide cohort study. J Prev Med Public Health. 2022;55:475–84.
pubmed: 36229910
pmcid: 9561145
doi: 10.3961/jpmph.22.286
Pasqual E, O’Brien K, Rinaldi S, Sandler DP, Kitahara CM. Obesity, obesity-related metabolic conditions, and risk of thyroid cancer in women: results from a prospective cohort study (Sister Study). Lancet Reg Health Am. 2023;23:100537.
pubmed: 37346380
pmcid: 10279535
Nguyen DN, Kim JH, Kim MK. Association of metabolic health and central obesity with the risk of thyroid cancer: data from the Korean Genome and Epidemiology Study. Cancer Epidemiol Biomark Prev. 2022;31:543–53.
doi: 10.1158/1055-9965.EPI-21-0255
Park B. Associations between obesity, metabolic syndrome, and endometrial cancer risk in East Asian women. J Gynecol Oncol. 2022;33:e35.
pubmed: 35320886
pmcid: 9250850
doi: 10.3802/jgo.2022.33.e35
Shao F, Chen Y, Xu H, Chen X, Zhou J, Wu Y, et al. Metabolic obesity phenotypes and risk of lung cancer: a prospective cohort study of 450,482 UK Biobank participants. Nutrients. 2022;14:3370.
Sun M, Fritz J, Haggstrom C, Bjorge T, Nagel G, Manjer J, et al. Metabolically (un)healthy obesity and risk of obesity-related cancers: a pooled study. J Natl Cancer Inst. 2023;115:456–67.
pubmed: 36647199
pmcid: 10086630
doi: 10.1093/jnci/djad008
Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535.
pubmed: 19622551
pmcid: 2714657
doi: 10.1136/bmj.b2535
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283:2008–12.
pubmed: 10789670
doi: 10.1001/jama.283.15.2008
Sterne JA, Hernan MA, Reeves BC, Savovic J, Berkman ND, Viswanathan M, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ. 2016;355:i4919.
pubmed: 27733354
pmcid: 5062054
doi: 10.1136/bmj.i4919
Schunemann HJ, Cuello C, Akl EA, Mustafa RA, Meerpohl JJ, Thayer K, et al. GRADE guidelines: 18. How ROBINS-I and other tools to assess risk of bias in nonrandomized studies should be used to rate the certainty of a body of evidence. J Clin Epidemiol. 2019;111:105–14.
pubmed: 29432858
doi: 10.1016/j.jclinepi.2018.01.012
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–88.
pubmed: 3802833
doi: 10.1016/0197-2456(86)90046-2
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. 2010;121:230–6.
pubmed: 20038741
doi: 10.1161/CIRCULATIONAHA.109.887521
Lin CJ, Chang YC, Hsu HY, Tsai MC, Hsu LY, Hwang LC, et al. Metabolically healthy overweight/obesity and cancer risk: a representative cohort study in Taiwan. Obes Res Clin Pr. 2021;15:564–9.
doi: 10.1016/j.orcp.2021.10.004
Hamling J, Lee P, Weitkunat R, Ambuhl M. Facilitating meta-analyses by deriving relative effect and precision estimates for alternative comparisons from a set of estimates presented by exposure level or disease category. Stat Med. 2008;27:954–70.
pubmed: 17676579
doi: 10.1002/sim.3013
Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58.
pubmed: 12111919
doi: 10.1002/sim.1186
Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–34.
pubmed: 9310563
pmcid: 2127453
doi: 10.1136/bmj.315.7109.629
Cho YK, Kim HS, Park JY, Lee WJ, Kim YJ, Jung CH. Implications of metabolic health status and obesity on the risk of kidney cancer: a nationwide population-based cohort study. Front Endocrinol. 2022;13:976056.
doi: 10.3389/fendo.2022.976056
Cho YK, Lee J, Kim HS, Park JY, Lee WJ, Kim YJ, et al. Metabolic health is a determining factor for incident colorectal cancer in the obese population: a nationwide population-based cohort study. Cancer Med. 2021;10:220–9.
pubmed: 33216467
doi: 10.1002/cam4.3607
Dibaba DT, Braithwaite D, Akinyemiju T. Metabolic syndrome and the risk of breast cancer and subtypes by race, menopause and BMI. Cancers. 2018;10:299.
Hashimoto Y, Hamaguchi M, Obora A, Kojima T, Fukui M. Impact of metabolically healthy obesity on the risk of incident gastric cancer: a population-based cohort study. BMC Endocr Disord. 2020;20:11.
pubmed: 31959179
pmcid: 6971909
doi: 10.1186/s12902-019-0472-2
Kabat GC, Kim MY, Lee JS, Ho GY, Going SB, Beebe-Dimmer J, et al. Metabolic obesity phenotypes and risk of breast cancer in postmenopausal women. Cancer Epidemiol Biomark Prev. 2017;26:1730–5.
doi: 10.1158/1055-9965.EPI-17-0495
Kim JW, Ahn ST, Oh MM, Moon DG, Cheon J, Han K, et al. Increased incidence of bladder cancer with metabolically unhealthy status: analysis from the National Health Checkup database in Korea. Sci Rep. 2020;10:6476.
pubmed: 32296103
pmcid: 7160147
doi: 10.1038/s41598-020-63595-3
Kwon H, Chang Y, Cho A, Ahn J, Park SE, Park CY, et al. Metabolic obesity phenotypes and thyroid cancer risk: a cohort study. Thyroid. 2019;29:349–58.
pubmed: 30648486
doi: 10.1089/thy.2018.0327
Liang X, Margolis KL, Hendryx M, Rohan TE, Groessl EJ, Thomson CA, et al. Metabolic phenotype and risk of colorectal cancer in normal-weight postmenopausal women. Cancer Epidemiol Biomark Prev. 2017;26:155–61.
doi: 10.1158/1055-9965.EPI-16-0761
Park JH, Choi M, Kim JH, Kim J, Han K, Kim B, et al. Metabolic syndrome and the risk of thyroid cancer: a nationwide population-based cohort study. Thyroid. 2020;30:1496–504.
pubmed: 32524894
doi: 10.1089/thy.2019.0699
Park YM, White AJ, Nichols HB, O’Brien KM, Weinberg CR, Sandler DP. The association between metabolic health, obesity phenotype and the risk of breast cancer. Int J Cancer. 2017;140:2657–66.
pubmed: 28268252
pmcid: 5406245
doi: 10.1002/ijc.30684
Reeves KW, McLaughlin V, Fredman L, Ensrud K, Cauley JA. Components of metabolic syndrome and risk of breast cancer by prognostic features in the study of osteoporotic fractures cohort. Cancer Causes Control. 2012;23:1241–51.
pubmed: 22661101
pmcid: 3576860
doi: 10.1007/s10552-012-0002-2
Shin CM, Han K, Lee DH, Choi YJ, Kim N, Park YS, et al. Association among obesity, metabolic health, and the risk for colorectal cancer in the general population in Korea using the National Health Insurance Service-National Sample Cohort. Dis Colon Rectum. 2017;60:1192–200.
pubmed: 28991084
doi: 10.1097/DCR.0000000000000876
Chappell J, Leitner JW, Solomon S, Golovchenko I, Goalstone ML, Draznin B. Effect of insulin on cell cycle progression in MCF-7 breast cancer cells. Direct and potentiating influence. J Biol Chem. 2001;276:38023–8.
pubmed: 11500498
doi: 10.1074/jbc.M104416200
Ish-Shalom D, Christoffersen CT, Vorwerk P, Sacerdoti-Sierra N, Shymko RM, Naor D, et al. Mitogenic properties of insulin and insulin analogues mediated by the insulin receptor. Diabetologia. 1997;40:S25–31.
pubmed: 9248698
doi: 10.1007/s001250051393
Perry RJ, Shulman GI. Mechanistic links between obesity, insulin, and cancer. Trends Cancer. 2020;6:75–8.
pubmed: 32061306
pmcid: 7214048
doi: 10.1016/j.trecan.2019.12.003
Farooqi IS, O’Rahilly S. Leptin: a pivotal regulator of human energy homeostasis. Am J Clin Nutr. 2009;89:980S–4S.
pubmed: 19211814
doi: 10.3945/ajcn.2008.26788C
Lejawa M, Osadnik K, Czuba Z, Osadnik T, Pawlas N. Association of metabolically healthy and unhealthy obesity phenotype with markers related to obesity, diabetes among young, healthy adult men. Analysis of MAGNETIC Study. Life. 2021;11:1350.
Housa D, Housova J, Vernerova Z, Haluzik M. Adipocytokines and cancer. Physiol Res. 2006;55:233–44.
pubmed: 16238454
doi: 10.33549/physiolres.930848
Sharma D, Saxena NK, Vertino PM, Anania FA. Leptin promotes the proliferative response and invasiveness in human endometrial cancer cells by activating multiple signal-transduction pathways. Endocr Relat Cancer. 2006;13:629–40.
pubmed: 16728588
pmcid: 2925427
doi: 10.1677/erc.1.01169
Yoon YS, Kwon AR, Lee YK, Oh SW. Circulating adipokines and risk of obesity related cancers: a systematic review and meta-analysis. Obes Res Clin Pr. 2019;13:329–39.
doi: 10.1016/j.orcp.2019.03.006
Ferreira FG, Reitz LK, Valmorbida A, Papini Gabiatti M, Hansen F, Faria Di Pietro P, et al. Metabolically unhealthy and overweight phenotypes are associated with increased levels of inflammatory cytokines: a population-based study. Nutrition. 2022;96:111590.
pubmed: 35180622
doi: 10.1016/j.nut.2022.111590
Dossus L, Lukanova A, Rinaldi S, Allen N, Cust AE, Becker S, et al. Hormonal, metabolic, and inflammatory profiles and endometrial cancer risk within the EPIC cohort-a factor analysis. Am J Epidemiol. 2013;177:787–99.
pubmed: 23492765
doi: 10.1093/aje/kws309
Heikkila K, Harris R, Lowe G, Rumley A, Yarnell J, Gallacher J, et al. Associations of circulating C-reactive protein and interleukin-6 with cancer risk: findings from two prospective cohorts and a meta-analysis. Cancer Causes Control. 2009;20:15–26.
pubmed: 18704713
doi: 10.1007/s10552-008-9212-z
Michels N, van Aart C, Morisse J, Mullee A, Huybrechts I. Chronic inflammation towards cancer incidence: a systematic review and meta-analysis of epidemiological studies. Crit Rev Oncol Hematol. 2021;157:103177.
pubmed: 33264718
doi: 10.1016/j.critrevonc.2020.103177
Deng T, Lyon CJ, Bergin S, Caligiuri MA, Hsueh WA. Obesity, inflammation, and cancer. Annu Rev Pathol. 2016;11:421–49.
pubmed: 27193454
doi: 10.1146/annurev-pathol-012615-044359
Stone TW, McPherson M, Gail Darlington L. Obesity and cancer: existing and new hypotheses for a causal connection. EBioMedicine. 2018;30:14–28.
pubmed: 29526577
pmcid: 5952217
doi: 10.1016/j.ebiom.2018.02.022
Stefan N, Kantartzis K, Machann J, Schick F, Thamer C, Rittig K, et al. Identification and characterization of metabolically benign obesity in humans. Arch Intern Med. 2008;168:1609–16.
pubmed: 18695074
doi: 10.1001/archinte.168.15.1609
Bluher M. Metabolically healthy obesity. Endocr Rev. 2020;41:bnaa004.
Slagter SN, Corpeleijn E, van der Klauw MM, Sijtsma A, Swart-Busscher LG, Perenboom CWM, et al. Dietary patterns and physical activity in the metabolically (un)healthy obese: the Dutch Lifelines cohort study. Nutr J. 2018;17:18.
pubmed: 29433580
pmcid: 5809859
doi: 10.1186/s12937-018-0319-0
Karra P, Winn M, Pauleck S, Bulsiewicz-Jacobsen A, Peterson L, Coletta A, et al. Metabolic dysfunction and obesity-related cancer: beyond obesity and metabolic syndrome. Obesity. 2022;30:1323–34.
pubmed: 35785479
doi: 10.1002/oby.23444
Cho YK, Kang YM, Yoo JH, Lee J, Park JY, Lee WJ, et al. Implications of the dynamic nature of metabolic health status and obesity on risk of incident cardiovascular events and mortality: a nationwide population-based cohort study. Metabolism. 2019;97:50–6.
pubmed: 31071310
doi: 10.1016/j.metabol.2019.05.002
Hamer M, Bell JA, Sabia S, Batty GD, Kivimaki M. Stability of metabolically healthy obesity over 8 years: the English Longitudinal Study of Ageing. Eur J Endocrinol. 2015;173:703–8.
pubmed: 26286585
doi: 10.1530/EJE-15-0449
Lee SH, Yang HK, Ha HS, Lee JH, Kwon HS, Park YM, et al. Changes in metabolic health status over time and risk of developing type 2 diabetes: a prospective cohort study. Medicine. 2015;94:e1705.
pubmed: 26448024
pmcid: 4616763
doi: 10.1097/MD.0000000000001705
NCD Risk Factor Collaboration. Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128.9 million children, adolescents, and adults. Lancet. 2017;390:2627–42.
doi: 10.1016/S0140-6736(17)32129-3