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Beneficial Short-Term Effects of Bariatric Surgery on Nutritional Inflammatory Profile and Metabolic Biomarkers

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Abstract

Purpose

Bariatric surgery (BS) has several potential metabolic benefits. However, little is known about its impact on changes in the inflammatory potential of diet and its effect on inflammatory and metabolic markers. This study aimed to assess the short-term beneficial effects of BS on dietary inflammatory potential and inflammatory and metabolic markers.

Materials and Methods

Participants (n = 20) were evaluated 3 months before and after BS. Body mass, body mass index, anthropometric measurements, fat mass, fat-free mass, visceral fat, skeletal muscle mass, basal metabolic rate, serum lipids, HOMA-IR, QUICKI and inflammatory markers, including leptin, adiponectin, adiponectin/leptin ratio and plasminogen activator inhibitor-1 (PAI-1), were evaluated. Diet data were collected using a 3-day diet record and the dietary inflammatory index (DII®) and energy-adjusted dietary inflammatory index (E-DIITM) scores were computed.

Results

There was a reduction in DII® (2.56 vs 2.13) and E-DIITM (2.18 vs 0.45) indicating an improvement in inflammatory nutritional profile. Moreover, there were increases in the adiponectin/leptin ratio (0.08 vs 0.21) and QUICKI scores (0.31 vs 0.37), and reductions in leptin (36.66 vs 11.41 ng/ml) and HOMA-IR scores (3.93 vs 1.50). There were also improvements in body composition and anthropometric parameters.

Conclusions

BS promotes changes in metabolic profile, inflammatory state and food intake and these modifications appeared to be associated with improvements in diet-related inflammation, an increase in the adiponectin/leptin ratio and a reduction in leptin. These results contribute to knowledge on the contribution bariatric surgery can make to the treatment of obesity and the reduction of related comorbidities.

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References

  1. Blüher M. Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol. 2019;15(5):288–98.

    Article  PubMed  Google Scholar 

  2. Chooi YC, Ding C, Magkos F. The epidemiology of obesity. Metabolism. 2019;92:6–10.

    Article  CAS  PubMed  Google Scholar 

  3. Perdomo CM, Cohen RV, Sumithran P, et al. Contemporary medical, device, and surgical therapies for obesity in adults. Lancet. 2023;S0140-6736(22):02403–5. https://doi.org/10.1016/S0140-6736(22)02403-5.

    Article  Google Scholar 

  4. Singh P, Subramanian A, Adderley N, et al. Impact of bariatric surgery on cardiovascular outcomes and mortality: a population-based cohort study. Br J Surg. 2020;107(4):432–42.

    Article  CAS  PubMed  Google Scholar 

  5. Park CH, Nam SJ, Choi HS, et al. Korean Research Group for endoscopic management of metabolic disorder and obesity. Comparative efficacy of bariatric surgery in the treatment of morbid obesity and diabetes mellitus: a systematic review and network meta-analysis. Obes Surg. 2019;29(7):2180–90.

    Article  PubMed  Google Scholar 

  6. Agarwal L, Aggarwal S, Shalimar YR, et al. Bariatric surgery in nonalcoholic fatty liver disease (NAFLD): impact assessment using paired liver biopsy and fibroscan. Obes Surg. 2021;31(2):617–26.

    Article  PubMed  Google Scholar 

  7. Latteri S, Sofia M, Puleo S, et al. Mechanisms linking bariatric surgery to adipose tissue, glucose metabolism, fatty liver disease and gut microbiota. Langenbecks Arch Surg. 2023;408(1):101.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Arterburn DE, Telem DA, Kushner RF, et al. Benefits and risks of bariatric surgery in adults: a review. JAMA. 2020;324(9):879–87.

    Article  PubMed  Google Scholar 

  9. Recarte M, Corripio R, Palma S, et al. Improvement of low-grade inflammation in patients with metabolically healthy severe obesity after primary bariatric surgery. Obes Surg. 2023;33(1):38–46.

    Article  PubMed  Google Scholar 

  10. Liu W, Zhou X, Li Y, et al. Serum leptin, resistin, and adiponectin levels in obese and non-obese patients with newly diagnosed type 2 diabetes mellitus: a population-based study. Medicine (Baltimore). 2020;99(6):e19052.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Barnard SA, Pieters M, De Lange Z. The contribution of different adipose tissue depots to plasma plasminogen activator inhibitor-1 (PAI-1) levels. Blood Rev. 2016;30(6):421–9.

    Article  CAS  PubMed  Google Scholar 

  12. Frühbeck G, Catalán V, Rodríguez A, et al. Involvement of the leptin-adiponectin axis in inflammation and oxidative stress in the metabolic syndrome. Sci Rep. 2017;7(1):6619.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Ouchi N, Parker JL, Lugus JJ, et al. Adipokines in inflammation and metabolic disease. Nat Rev Immunol. 2011;11(2):85–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Namazi N, Larijani B, Azadbakht L. Dietary inflammatory index and its association with the risk of cardiovascular diseases, metabolic syndrome, and mortality: a systematic review and meta-analysis. Horm Metab Res. 2018;50(5):345–58.

    Article  CAS  PubMed  Google Scholar 

  15. Shivappa N, Hebert JR, Marcos A, et al. Association between dietary inflammatory index and inflammatory markers in the HELENA study. Mol Nutr Food Res. 2017;61(6):1600707. https://doi.org/10.1002/mnfr.201600707.

    Article  CAS  Google Scholar 

  16. Shivappa N, Steck SE, Hurley TG, et al. Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr. 2014;17(8):1689–96.

    Article  PubMed  Google Scholar 

  17. Marx W, Veronese N, Kelly JT, et al. The dietary inflammatory index and human health: an umbrella review of meta-analyses of observational studies. Adv Nutr. 2021;12(5):1681–90.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Khan I, Kwon M, Shivappa N, et al. Positive association of dietary inflammatory index with incidence of cardiovascular disease: findings from a Korean population-based prospective study. Nutrients. 2020;12(2):588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Zahedi H, Djalalinia S, Asayesh H, et al. A higher dietary inflammatory index score is associated with a higher risk of incidence and mortality of cancer: a comprehensive systematic review and meta-analysis. Int J Prev Med. 2020;17(11):15.

    Google Scholar 

  20. Phillips CM, Chen LW, Heude B, et al. Dietary inflammatory index and non-communicable disease risk: a narrative review. Nutrients. 2019;11(8):1873.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Shivappa N, Godos J, Hébert JR, et al. Dietary inflammatory index and cardiovascular risk and mortality-a meta-analysis. Nutrients. 2018;10(2):200.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Andrade PA, Hermsdorff HHM, Leite JIA, et al. Baseline pro-inflammatory diet is inversely associated with change in weight and body fat 6 months following-up to bariatric surgery. Obes Surg. 2019;29(2):457–63.

    Article  PubMed  Google Scholar 

  23. Pinto SL, Juvanhol LL, da Silva A, et al. The preoperative dietary inflammatory index predicts changes in cardiometabolic risk factors after 12 months of Roux-en-Y gastric bypass. Obes Surg. 2020;30(10):3932–9.

    Article  PubMed  Google Scholar 

  24. Martinho FL, Tangerina RP, Moura SM, et al. Systematic head and neck physical examination as a predictor of obstructive sleep apnea in class III obese patients. Braz J Med Biol Res. 2008;41(12):1093–7.

    Article  CAS  PubMed  Google Scholar 

  25. Nishida C, Ko GT, Kumanyika S. Body fat distribution and noncommunicable diseases in populations: overview of the 2008 WHO Expert Consultation on Waist Circumference and Waist-Hip Ratio. Eur J Clin Nutr. 2010;64(1):2–5.

    Article  CAS  PubMed  Google Scholar 

  26. Nelson KM, Weinsier RL, Long CL, et al. Prediction of resting energy expenditure from fat-free mass and fat mass. Am J Clin Nutr. 1992;56(5):848–56.

    Article  CAS  PubMed  Google Scholar 

  27. Katz A, Nambi SS, Mather K, et al. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab. 2000;85(7):2402–10.

    Article  CAS  PubMed  Google Scholar 

  28. Geloneze B, Repetto EM, Geloneze SR, et al. The threshold value for insulin resistance (HOMA-IR) in an admixtured population IR in the Brazilian Metabolic Syndrome Study. Diabetes Res Clin Pract. 2006;72(2):219–20.

    Article  CAS  PubMed  Google Scholar 

  29. Hébert JR, Shivappa N, Wirth MD, et al. Perspective: the dietary inflammatory index (DII)-lessons learned, improvements made, and future directions. Adv Nutr. 2019;10(2):185–95.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Harmon B, Wirth M, Boushey C, et al. The dietary inflammatory index is associated with colorectal cancer risk in the multiethnic cohort. J Nutr. 2017;147:430–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Carraro JC, Hermsdorff HH, Mansego ML, et al. Higher fruit intake is related to TNF-α hypomethylation and better glucose tolerance in healthy subjects. J Nutrigenet Nutrigenomics. 2016;9(2-4):95–105.

    CAS  PubMed  Google Scholar 

  32. Sezavar H, Yousefi R, Abbasi M, et al. Anthropometric and biochemical measures in bariatric surgery candidates: what is the role of inflammatory potential of diet? Obes Surg. 2021;31(7):3097–108.

    Article  PubMed  Google Scholar 

  33. Pan WW, Myers Jr MG. Leptin and the maintenance of elevated body weight. Nat Rev Neurosci. 2018;19(2):95–105.

    Article  CAS  PubMed  Google Scholar 

  34. Mechanick JI, Zhao S, Garvey WT. Leptin, An adipokine with central importance in the global obesity problem. Glob Heart. 2018;13(2):113–27.

    Article  PubMed  Google Scholar 

  35. Gómez-Ambrosi J, Salvador J, Páramo JA, et al. Involvement of leptin in the association between percentage of body fat and cardiovascular risk factors. Clin Biochem. 2002;35(4):315–20.

    Article  PubMed  Google Scholar 

  36. Lambert G, Lima MMO, Felici AC, et al. Early regression of carotid intima-media thickness after bariatric surgery and its relation to serum leptin reduction. Obes Surg. 2018;28(1):226–33.

    Article  CAS  PubMed  Google Scholar 

  37. Barragán-Vázquez S, Ariza AC, Ramírez Silva I, et al. Pro-inflammatory diet is associated with adiposity during childhood and with adipokines and inflammatory markers at 11 years in Mexican children. Nutrients. 2020;12(12):3658.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Muhammad HFL, van Baak MA, Mariman EC, et al. Dietary inflammatory index score and its association with body weight, blood pressure, lipid profile, and leptin in Indonesian adults. Nutrients. 2019;11(1):148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Farias G, Silva RMO, da Silva PPP, et al. Impact of dietary patterns according to NOVA food groups: 2 y after Roux-en-Y gastric bypass surgery. Nutrition. 2020;74:110746.

    Article  CAS  PubMed  Google Scholar 

  40. Frühbeck G, Catalán V, Rodríguez A, et al. Adiponectin-leptin ratio is a functional biomarker of adipose tissue inflammation. Nutrients. 2019;11(2):454. https://doi.org/10.3390/nu11020454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hosseinzadeh-Attar MJ, Golpaie A, Janani L, et al. Effect of weight reduction following bariatric surgery on serum visfatin and adiponectin levels in morbidly obese subjects. Obes Facts. 2013;6(2):193–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Valenzano A, Tartaglia N, Ambrosi A, et al. The metabolic rearrangements of bariatric surgery: focus on Orexin-A and the adiponectin system. J Clin Med. 2020;9(10):3327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Illán Gómez F, Gonzálvez Ortega M, Aragón Alonso A, et al. Obesity, endothelial function and inflammation: the effects of weight loss after bariatric surgery. Nutr Hosp. 2016;33(6):1340–6.

    Article  PubMed  Google Scholar 

  44. Poulain-Godefroy O, Lecoeur C, Pattou F, et al. Inflammation is associated with a decrease of lipogenic factors in omental fat in women. Am J Physiol Regul Integr Comp Physiol. 2008;295(1):R1–7.

    Article  CAS  PubMed  Google Scholar 

  45. Frühbeck G, Busetto L, Dicker D, et al. The ABCD of obesity: an EASO position statement on a diagnostic term with clinical and scientific implications. Obes Facts. 2019;12(2):131–6.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Choi JW, Park JS, Lee CH. Interactive effect of high sodium intake with increased serum triglycerides on hypertension. PLoS One. 2020;15(4):e0231707.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Lu M, Wan Y, Yang B, et al. Effects of low-fat compared with high-fat diet on cardiometabolic indicators in people with overweight and obesity without overt metabolic disturbance: a systematic review and meta-analysis of randomised controlled trials. Br J Nutr. 2018;119(1):96–108.

    Article  CAS  PubMed  Google Scholar 

  48. Jam SA, Rezaeian S, Najafi F, et al. Association of a pro-inflammatory diet with type 2 diabetes and hypertension: results from the Ravansar non-communicable diseases cohort study. Arch Public Health. 2022;80(1):102.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Tan J, Liu N, Sun P, et al. A proinflammatory diet may increase mortality risk in patients with diabetes mellitus. Nutrients. 2022;14(10):2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Institute of Medicine. Dietary reference intakes: the essential guide to nutrient requirements. Washington, DC: The National Academies Press; 2006. https://doi.org/10.17226/11537.

    Book  Google Scholar 

  51. Biobaku F, Ghanim H, Batra M, et al. Macronutrient-mediated inflammation and oxidative stress: relevance to insulin resistance, obesity, and atherogenesis. J Clin Endocrinol Metab. 2019;104(12):6118–28.

    Article  PubMed  Google Scholar 

  52. Salazar MR, Carbajal HA, Espeche WG, et al. Comparison of the abilities of the plasma triglyceride/high-density lipoprotein cholesterol ratio and the metabolic syndrome to identify insulin resistance. Diab Vasc Dis Res. 2013;10(4):346–52.

    Article  PubMed  Google Scholar 

  53. Lemieux I, Lamarche B, Couillard C, et al. Total cholesterol/HDL cholesterol ratio vs LDL cholesterol/HDL cholesterol ratio as indices of ischemic heart disease risk in men: the Quebec Cardiovascular Study. Arch Intern Med. 2001;161(22):2685–92.

    Article  CAS  PubMed  Google Scholar 

  54. Manninen V, Tenkanen L, Koskinen P, et al. Joint effects of serum triglyceride and LDL cholesterol and HDL cholesterol concentrations on coronary heart disease risk in the Helsinki Heart Study. Implications for treatment. Circulation. 1992;85(1):37–45.

    Article  CAS  PubMed  Google Scholar 

  55. Lira NS, Macedo CES, Belo GM, et al. Analysis of the lipid profile of patients submitted to sleeve gastrectomy and Roux-en-Y gastric bypass. Rev Col Bras Cir. 2018;45(6):e1967.

    PubMed  Google Scholar 

  56. Gero D, Favre L, Allemann P, et al. Laparoscopic Roux-En-Y gastric bypass improves lipid profile and decreases cardiovascular risk: a 5-year longitudinal cohort study of 1048 patients. Obes Surg. 2018;28(3):805–11.

    Article  PubMed  Google Scholar 

  57. Fakhry TK, Mhaskar R, Schwitalla T, et al. Bariatric surgery improves nonalcoholic fatty liver disease: a contemporary systematic review and meta-analysis. Surg Obes Relat Dis. 2019;15(3):502–11.

    Article  PubMed  Google Scholar 

  58. Nickel F, Tapking C, Benner L, et al. Bariatric surgery as an efficient treatment for non-alcoholic fatty liver disease in a prospective study with 1-year follow-up: BariScan Study. Obes Surg. 2018;28(5):1342–50.

    Article  PubMed  Google Scholar 

  59. Lautenbach A, Wernecke M, Riedel N, et al. Adaptive changes in pancreas post Roux-en-Y gastric bypass induced weight loss. Diabetes Metab Res Rev. 2018;34(7):e3025.

    Article  CAS  PubMed  Google Scholar 

  60. Preis SR, Massaro JM, Robins SJ, et al. Abdominal subcutaneous and visceral adipose tissue and insulin resistance in the Framingham heart study. Obesity (Silver Spring). 2010;18(11):2191–8.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Auclair A, Biertho L, Marceau S, et al. Bariatric surgery-induced resolution of hypertension and obstructive sleep apnea: impact of modulation of body fat, ectopic fat, autonomic nervous activity, inflammatory and adipokine profiles. Obes Surg. 2017;27(12):3156–64.

    PubMed  Google Scholar 

  62. Kim JH, Choi KH, Kang KW, et al. Impact of visceral adipose tissue on clinical outcomes after acute ischemic stroke. Stroke. 2019;50(2):448–54.

    Article  PubMed  Google Scholar 

  63. Lê KA, Mahurkar S, Alderete TL, et al. Subcutaneous adipose tissue macrophage infiltration is associated with hepatic and visceral fat deposition, hyperinsulinemia, and stimulation of NF-κB stress pathway. Diabetes. 2011;60(11):2802–9.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Muruzábal FJ, Frühbeck G, Gómez-Ambrosi J, et al. Immunocytochemical detection of leptin in non-mammalian vertebrate stomach. Gen Comp Endocrinol. 2002;128(2):149–52.

    Article  PubMed  Google Scholar 

  65. Rodríguez A, Gómez-Ambrosi J, Catalán V, et al. The ghrelin O-acyltransferase-ghrelin system reduces TNF-α-induced apoptosis and autophagy in human visceral adipocytes. Diabetologia. 2012;55(11):3038–50.

    Article  PubMed  Google Scholar 

  66. Kenngott HG, Nickel F, Wise PA, et al. Weight loss and changes in adipose tissue and skeletal muscle volume after laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass: a prospective study with 12-month follow-up. Obes Surg. 2019;29(12):4018–28.

    Article  PubMed  Google Scholar 

  67. Moriconi D, Nannipieri M, Dadson P, et al. The beneficial effects of bariatric-surgery-induced weight loss on renal function. Metabolites. 2022;12(10):967.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Coral RV, Bigolin AV, Machry MC, et al. Improvement in muscle strength and metabolic parameters despite muscle mass loss in the initial six months after bariatric surgery. Obes Surg. 2021;31(10):4485–91.

    Article  PubMed  Google Scholar 

  69. In G, Taskin HE, Al M, et al. Comparison of 12-week fitness protocols following bariatric surgery: aerobic exercise versus aerobic exercise and progressive resistance. Obes Surg. 2021;31(4):1475–84.

    Article  PubMed  Google Scholar 

  70. de Cleva R, Mota FC, Gadducci AV, et al. Resting metabolic rate and weight loss after bariatric surgery. Surg Obes Relat Dis. 2018;14(6):803–7.

    Article  PubMed  Google Scholar 

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Funding

Support Foundation of São Paulo Research - FAPESP (#2018/15921-8), Associação Fundo de Incentivo à Pesquisa - AFIP, National Council for Scientific and Technological Development - CNPq, and Coordination of Higher Education Personnel Training - CAPES.

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Authors

Contributions

Danielle Cristina Seva (A, B, C and D); Marcos Mônico-Neto (A, B, C and D); Hanna Karen Moreira Antunes (A, B, C and D); Jessica Monteiro Volejnik Pino (A, B, C and D); Lia Rita Azeredo Bittencourt (A, B, C and D); Thales Delmondes Galvão (A, B, C and D); Ana R. Dâmaso (A, B, C and D); Lila Missae Oyama (A, B, C and D); Nitin Shivappa (A, B, C and D); James R. Hébert (A, B, C and D); Sergio Tufik (A, B, C and D); Raquel Munhoz da Silveira Campos (A, B, C and D)

A—Substantial contributions to the conception or design of the work; or the acquisition, analysis, or interpretation of data for the work;

B—Drafting the work or revising it critically for important intellectual content;

C—Final approval of the version to be published;

D—Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Marcos Mônico-Neto.

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Ethics approval

This study was conducted under the principles of the 1964 Helsinki Declaration and was approved by the Research Ethics Committee.

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Informed consent was obtained from all individual participants included in the study.

Conflict of Interest

Dr. James R. Hébert owns controlling interest in Connecting Health Innovations LLC (CHI), a company that has licensed the right to his invention of the dietary inflammatory index (DII®) from the University of South Carolina in order to develop computer and smart phone applications for patient counseling and dietary intervention in clinical settings. Dr. Nitin Shivappa is an employee of CHI. The subject matter of this paper will not have any direct bearing on that work, nor has that activity exerted any influence on this project.

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Key Points

• Bariatric surgery improves metabolic state

• Positive effects in dietary inflammatory profile occur after bariatric surgery

• Increase in the adiponectin/leptin ratio and a reduction in leptin occur after bariatric surgery

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Seva, D.C., Mônico-Neto, M., Antunes, H.K.M. et al. Beneficial Short-Term Effects of Bariatric Surgery on Nutritional Inflammatory Profile and Metabolic Biomarkers. OBES SURG 33, 2789–2798 (2023). https://doi.org/10.1007/s11695-023-06743-8

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