Skip to main content

Advertisement

Log in

Effect of Bariatric Surgery on Serum Inflammatory Factors of Obese Patients: a Systematic Review and Meta-Analysis

  • Review Article
  • Published:
Obesity Surgery Aims and scope Submit manuscript

Abstract

Obesity is one of the main causes of inflammation. Previous studies have reported inconclusive results regarding the effect of bariatric surgery on inflammatory markers. This systematic review and meta-analysis is aimed at describing the effect of bariatric surgery on C-reactive protein (CRP), interleukin-6 (IL-6), tumor necrosis factor-α (TNF-α). PubMed/Medline and Scopus were systematically searched for all eligible studies from inception to June 2018. Results are expressed as weighted mean difference (MD) with 95% confidence intervals (CI) using a random effects model. Overall, 116 studies which evaluated serum CRP, IL-6, and TNF-α after bariatric surgery were included. Pooled effect size showed significant reduction in serum CRP (− 5.30 mg/l, 95% CI − 5.46, − 5.15, P < 0.001), IL-6 (− 0.58 pg/ml, 95% CI − 0.64, − 0.53, P < 0.001), and TNF-α (− 0.20 pg/ml, 95% CI − 0.39, − 0.02, P = 0.031) with significant heterogeneity across studies (> 95% for all factors). Bariatric surgery significantly lowered inflammatory factors; however, baseline BMI, follow-up duration and type of surgery could impact the extent of observed effects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. James, Philip T., Neville Rigby, Rachel Leach, and International Obesity Task Force. "The obesity epidemic, metabolic syndrome and future prevention strategies." Eur. J. Cardiovasc. Prev. Rehabil. 2004;11(1): 3–8.

  2. Cai H, Shu XO, Gao YT, et al. A prospective study of dietary patterns and mortality in Chinese women. Epidemiology (Cambridge, Mass). 2007;18(3):393–401. https://doi.org/10.1097/01.ede.0000259967.21114.45.

    Article  Google Scholar 

  3. Faith MS, Butryn M, Wadden TA, et al. Evidence for prospective associations among depression and obesity in population-based studies. Obes Rev. 2011;12(5):e438–53. https://doi.org/10.1111/j.1467-789X.2010.00843.x.

    Article  CAS  PubMed  Google Scholar 

  4. MacLean PS, Wing RR, Davidson T, et al. NIH working group report: innovative research to improve maintenance of weight loss. Obesity (Silver Spring, Md). 2015;23(1):7–15. https://doi.org/10.1002/oby.20967.

    Article  Google Scholar 

  5. Madura 2nd JA, Dibaise JK. Quick fix or long-term cure? Pros and cons of bariatric surgery. F1000 Med Re. 2012;4:19. https://doi.org/10.3410/m4-19.

    Article  Google Scholar 

  6. Tham JC, Howes N, le Roux CW. The role of bariatric surgery in the treatment of diabetes. Ther Adv Chronic Dis. 2014;5(3):149–57. https://doi.org/10.1177/2040622313513313.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Courcoulas AP, Yanovski SZ, Bonds D, et al. Long-term outcomes of bariatric surgery: a National Institutes of Health symposium. JAMA Surg. 2014;149(12):1323–9. https://doi.org/10.1001/jamasurg.2014.2440.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Xanthakos SA. Nutritional deficiencies in obesity and after bariatric surgery. Pediatr Clin N Am. 2009;56(5):1105–21. https://doi.org/10.1016/j.pcl.2009.07.002.

    Article  Google Scholar 

  9. Tice JA, Karliner L, Walsh J, et al. Gastric banding or bypass? A systematic review comparing the two most popular bariatric procedures. Am J Med. 2008;121(10):885–93. https://doi.org/10.1016/j.amjmed.2008.05.036.

    Article  PubMed  Google Scholar 

  10. Viégas M, Vasconcelos RS, Neves AP, et al. Bariatric surgery and bone metabolism: a systematic review. Arq Bras Endocrinol Metabol. 2010;54:158–63.

    PubMed  Google Scholar 

  11. Whitson JM, Stackhouse GB, Stoller ML. Hyperoxaluria after modern bariatric surgery: case series and literature review. Int Urol Nephrol. 2010;42(2):369–74. https://doi.org/10.1007/s11255-009-9602-5.

    Article  PubMed  Google Scholar 

  12. Ferrero-Miliani L, Nielsen OH, Andersen PS, et al. Chronic inflammation: importance of NOD2 and NALP3 in interleukin-1β generation. Clin Exp Immunol. 2007;147(2):227–35. https://doi.org/10.1111/j.1365-2249.2006.03261.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Galli SJ, Tsai M, Piliponsky AM. The development of allergic inflammation. Nature. 2008;454(7203):445–54. https://doi.org/10.1038/nature07204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Jeong YJ, Oh HK, Park SH, et al. Association between inflammation and cancer stem cell phenotype in breast cancer. Oncol Lett. 2018;15(2):2380–6. https://doi.org/10.3892/ol.2017.7607.

    Article  CAS  PubMed  Google Scholar 

  15. Greenfield JR, Campbell LV. Relationship between inflammation, insulin resistance and type 2 diabetes: ‘cause or effect’? Curr Diabetes Rev. 2006;2(2):195–211.

    CAS  PubMed  Google Scholar 

  16. Libby P. History of discovery: inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol. 2012;32(9):2045–51. https://doi.org/10.1161/ATVBAHA.108.179705.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chimenti MS, Triggianese P, Conigliaro P, et al. The interplay between inflammation and metabolism in rheumatoid arthritis. Cell Death Dis. 2015;6(9):e1887. https://doi.org/10.1038/cddis.2015.246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bautista LE, Vera LM, Arenas IA, et al. Independent association between inflammatory markers (C-reactive protein, interleukin-6, and TNF-alpha) and essential hypertension. J Hum Hypertens. 2005;19(2):149–54. https://doi.org/10.1038/sj.jhh.1001785.

    Article  CAS  PubMed  Google Scholar 

  19. Ellulu MS, Patimah I, Khaza’ai H, et al. Obesity and inflammation: the linking mechanism and the complications. Arch Med Sci. 2017;13(4):851–63. https://doi.org/10.5114/aoms.2016.58928.

    Article  CAS  PubMed  Google Scholar 

  20. Lafontan M. Fat cells: afferent and efferent messages define new approaches to treat obesity. Annu Rev Pharmacol Toxicol. 2005;45:119–46. https://doi.org/10.1146/annurev.pharmtox.45.120403.095843.

    Article  CAS  PubMed  Google Scholar 

  21. Ganter U, Arcone R, Toniatti C, et al. Dual control of C-reactive protein gene expression by interleukin-1 and interleukin-6. EMBO J. 1989;8(12):3773–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097. https://doi.org/10.1371/journal.pmed.1000097.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Wells G, Shea B, O’connell D, et al. The Newcastle-Ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa: Dept of Epidemiology and Community Medicine, University of Ottawa; 2011.

    Google Scholar 

  24. Wells GASB. The Newcastle Ottawa scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. 2011. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp

  25. Borenstein M, Hedges LV, Higgins JP, et al. Introduction to meta-analysis. Hoboken: Wiley; 2011.

    Google Scholar 

  26. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ: Br Med J. 2003;327(7414):557–60.

    Google Scholar 

  27. Carroll JF, Franks SF, Smith AB, et al. Visceral adipose tissue loss and insulin resistance 6 months after laparoscopic gastric banding surgery: a preliminary study. Obes Surg. 2009;19(1):47–55.

    Article  PubMed  Google Scholar 

  28. Schmatz R, Bitencourt MR, Patias LD, et al. Evaluation of the biochemical, inflammatory and oxidative profile of obese patients given clinical treatment and bariatric surgery. Clin Chim Acta. 2017;465:72–9. https://doi.org/10.1016/j.cca.2016.12.012.

    Article  CAS  PubMed  Google Scholar 

  29. Nerla R, Tarzia P, Sestito A, et al. Effect of bariatric surgery on peripheral flow-mediated dilation and coronary microvascular function. Nutr Metab Cardiovasc Dis. 2012;22(8):626–34. https://doi.org/10.1016/j.numecd.2010.10.004.

    Article  CAS  PubMed  Google Scholar 

  30. Boulet LP, Turcotte H, Martin J, et al. Effect of bariatric surgery on airway response and lung function in obese subjects with asthma. Respir Med. 2012;106(5):651–60. https://doi.org/10.1016/j.rmed.2011.12.012.

    Article  PubMed  Google Scholar 

  31. Cheng V, Kashyap SR, Schauer PR, et al. Restoration of glycemic control in patients with type 2 diabetes mellitus after bariatric surgery is associated with reduction in microparticles. Surg Obes Relat Dis. 2013;9(2):207–12. https://doi.org/10.1016/j.soard.2011.09.026.

    Article  PubMed  Google Scholar 

  32. Garrido-Sanchez L, Tome M, Santiago-Fernandez C, et al. Adipose tissue biomarkers involved in early resolution of type 2 diabetes after bariatric surgery. Surg Obes Relat Dis. 2017;13(1):70–7. https://doi.org/10.1016/j.soard.2016.03.010.

    Article  PubMed  Google Scholar 

  33. Lips MA, Pijl H, Van Klinken JB, et al. Roux-en-Y gastric bypass and calorie restriction induce comparable time-dependent effects on thyroid hormone function tests in obese female subjects. Eur J Endocrinol. 2013;169(3):339–47. https://doi.org/10.1530/EJE-13-0339.

    Article  CAS  PubMed  Google Scholar 

  34. Lips MA, van Klinken JB, Pijl H, et al. Weight loss induced by very low calorie diet is associated with a more beneficial systemic inflammatory profile than by Roux-en-Y gastric bypass. Metab Clin Exp. 2016;65(11):1614–20. https://doi.org/10.1016/j.metabol.2016.07.013.

    Article  CAS  PubMed  Google Scholar 

  35. Shih KC, Janckila AJ, Lee WJ, et al. Effects of bariatric weight loss surgery on glucose metabolism, inflammatory cytokines, and serum tartrate-resistant acid phosphatase 5a in obese Chinese adults. Clin Chim Acta. 2016;453:197–202. https://doi.org/10.1016/j.cca.2015.11.004.

    Article  CAS  PubMed  Google Scholar 

  36. Jimenez A, Perea V, Corcelles R, et al. Metabolic effects of bariatric surgery in insulin-sensitive morbidly obese subjects. Obes Surg. 2013;23(4):494–500. https://doi.org/10.1007/s11695-012-0817-7.

    Article  PubMed  Google Scholar 

  37. van Huisstede A, Rudolphus A, Cabezas MC, Biter LU, van de Geijn G-J, Taube C, et al. Effect of bariatric surgery on asthma control, lung function and bronchial and systemic inflammation in morbidly obese subjects with asthma. Thorax. 2015;70(7):659-67.

    PubMed  Google Scholar 

  38. Komorowski J, Jankiewicz-Wika J, Kolomecki K, et al. Systemic blood osteopontin, endostatin, and E-selectin concentrations after vertical banding surgery in severely obese adults. Cytokine. 2011;55(1):56–61. https://doi.org/10.1016/j.cyto.2011.03.020.

    Article  CAS  PubMed  Google Scholar 

  39. Lima MM, Pareja JC, Alegre SM, et al. Acute effect of roux-en-y gastric bypass on whole-body insulin sensitivity: a study with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab. 2010;95(8):3871–5.

    CAS  PubMed  Google Scholar 

  40. Lin L-Y, Lee W-J, Shen H-N, et al. Nitric oxide production is paradoxically decreased after weight reduction surgery in morbid obesity patients. Atherosclerosis. 2007;190(2):436–42.

    CAS  PubMed  Google Scholar 

  41. Magro DO, Cazzo E, Kotze PG, et al. Glucose metabolism parameters and post-prandial GLP-1 and GLP-2 release largely vary in several distinct situations: a controlled comparison among individuals with Crohn’s disease and individuals with obesity before and after bariatric surgery. Obes Surg. 2018;28(2):378–88.

    PubMed  Google Scholar 

  42. Tussing-Humphreys LM, Nemeth E, Fantuzzi G, et al. Decreased serum hepcidin and improved functional iron status 6 months after restrictive bariatric surgery. Obesity. 2010;18(10):2010–6.

    CAS  PubMed  Google Scholar 

  43. Tussing-Humphreys L, Pini M, Ponemone V, et al. Suppressed cytokine production in whole blood cultures may be related to iron status and hepcidin and is partially corrected following weight reduction in morbidly obese pre-menopausal women. Cytokine. 2011;53(2):201–6. https://doi.org/10.1016/j.cyto.2010.11.008.

    Article  CAS  PubMed  Google Scholar 

  44. Sdralis E, Argentou M, Mead N, et al. A prospective randomized study comparing patients with morbid obesity submitted to sleeve gastrectomy with or without omentectomy. Obes Surg. 2013;23(7):965–71. https://doi.org/10.1007/s11695-013-0925-z.

    Article  PubMed  Google Scholar 

  45. Swarbrick M, Stanhope K, Austrheim-Smith I, et al. Longitudinal changes in pancreatic and adipocyte hormones following Roux-en-Y gastric bypass surgery. Diabetologia. 2008;51(10):1901–11.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Lin E, Phillips LS, Ziegler TR, et al. Increases in adiponectin predict improved liver, but not peripheral, insulin sensitivity in severely obese women during weight loss. Diabetes. 2007;56(3):735–42.

    CAS  PubMed  Google Scholar 

  47. Chacon M, Miranda M, Jensen C, et al. Human serum levels of fetal antigen 1 (FA1/Dlk1) increase with obesity, are negatively associated with insulin sensitivity and modulate inflammation in vitro. Int J Obes. 2008;32(7):1122–9.

    CAS  Google Scholar 

  48. Broch M, Gómez JM, Auguet MT, et al. Association of retinol-binding protein-4 (RBP4) with lipid parameters in obese women. Obes Surg. 2010;20(9):1258–64.

    PubMed  Google Scholar 

  49. Botella-Carretero JI, Álvarez-Blasco F, Martinez-García MÁ, et al. The decrease in serum IL-18 levels after bariatric surgery in morbidly obese women is a time-dependent event. Obes Surg. 2007;17(9):1199–208.

    PubMed  Google Scholar 

  50. Simón I, Escoté X, Vilarrasa N, et al. Adipocyte fatty acid-binding protein as a determinant of insulin sensitivity in morbid-obese women. Obesity. 2009;17(6):1124–8.

    PubMed  Google Scholar 

  51. Auguet T, Terra X, Hernandez M, et al. Clinical and adipocytokine changes after bariatric surgery in morbidly obese women. Obesity (Silver Spring). 2014;22(1):188–94. https://doi.org/10.1002/oby.20470.

    Article  CAS  Google Scholar 

  52. Illan-Gomez F, Gonzalvez-Ortega M, Orea-Soler I, et al. Obesity and inflammation: change in adiponectin, C-reactive protein, tumour necrosis factor-alpha and interleukin-6 after bariatric surgery. Obes Surg. 2012;22(6):950–5. https://doi.org/10.1007/s11695-012-0643-y.

    Article  PubMed  Google Scholar 

  53. Cintra W, Modolin M, Faintuch J, et al. C-reactive protein decrease after postbariatric abdominoplasty. Inflammation. 2012;35(1):316–20. https://doi.org/10.1007/s10753-011-9321-9.

    Article  CAS  PubMed  Google Scholar 

  54. Alili R, Nivet-Antoine V, Saldmann A, et al. Human catalase gene promoter haplotype and cardiometabolic improvement after bariatric surgery. Gene. 2018;656:17–21.

    CAS  PubMed  Google Scholar 

  55. Capuron L, Poitou C, Machaux-Tholliez D, et al. Relationship between adiposity, emotional status and eating behaviour in obese women: role of inflammation. Psychol Med. 2011;41(7):1517–28.

    CAS  PubMed  Google Scholar 

  56. Kopp H-P, Krzyzanowska K, Schernthaner G-H, et al. Relationship of androgens to insulin resistance and chronic inflammation in morbidly obese premenopausal women: studies before and after vertical banded gastroplasty. Obes Surg. 2006;16(9):1214–20.

    PubMed  Google Scholar 

  57. Schaller G, Aso Y, Schernthaner G-H, et al. Increase of osteopontin plasma concentrations after bariatric surgery independent from inflammation and insulin resistance. Obes Surg. 2009;19(3):351–6.

    PubMed  Google Scholar 

  58. Manco M, Fernandez-Real JM, Equitani F, et al. Effect of massive weight loss on inflammatory adipocytokines and the innate immune system in morbidly obese women. J Clin Endocrinol Metab. 2006;92(2):483–90.

    PubMed  Google Scholar 

  59. Cugno M, Castelli R, Mari D, et al. Inflammatory and prothrombotic parameters in normotensive non-diabetic obese women: effect of weight loss obtained by gastric banding. Intern Emerg Med. 2012;7(3):237–42.

    PubMed  Google Scholar 

  60. Silva-Nunes J, Oliveira A, Duarte L, et al. Factors related with adiponectinemia in obese and normal-weight women and with its variation in weight loss programs. Obes Facts. 2013;6(2):124–33. https://doi.org/10.1159/000350664.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Blum A, Tamir S, Hazzan D, et al. Gender effect on vascular inflammation following bariatric surgery. Eur Cytokine Netw. 2012;23(4):154–7.

    CAS  PubMed  Google Scholar 

  62. Marantos G, Daskalakis M, Karkavitsas N, et al. Changes in metabolic profile and adipoinsular axis in morbidly obese premenopausal females treated with restrictive bariatric surgery. World J Surg. 2011;35(9):2022–3. https://doi.org/10.1007/s00268-011-1165-9.

    Article  PubMed  Google Scholar 

  63. Dillard TH, Purnell JQ, Smith MD, et al. Omentectomy added to Roux-en-Y gastric bypass surgery: a randomized, controlled trial. Surg Obes Relat Dis. 2013;9(2):269–75. https://doi.org/10.1016/j.soard.2011.09.027.

    Article  PubMed  Google Scholar 

  64. Sams VG, Blackledge C, Wijayatunga N, et al. Effect of bariatric surgery on systemic and adipose tissue inflammation. Surg Endosc. 2016;30(8):3499–504. https://doi.org/10.1007/s00464-015-4638-3.

    Article  PubMed  Google Scholar 

  65. Belligoli A, Sanna M, Serra R, et al. Incidence and predictors of hypoglycemia 1 year after laparoscopic sleeve gastrectomy. Obes Surg. 2017;27(12):3179–86. https://doi.org/10.1007/s11695-017-2742-2.

    Article  PubMed  Google Scholar 

  66. Appachi S, Kelly KR, Schauer PR, et al. Reduced cardiovascular risk following bariatric surgeries is related to a partial recovery from “adiposopathy”. Obes Surg. 2011;21(12):1928–36. https://doi.org/10.1007/s11695-011-0447-5.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Miller GD, Nicklas BJ, Fernandez A. Serial changes in inflammatory biomarkers after Roux-en-Y gastric bypass surgery. Surg Obes Relat Dis. 2011;7(5):618–24. https://doi.org/10.1016/j.soard.2011.03.006.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Hawkins MA, Alosco ML, Spitznagel MB, et al. The association between reduced inflammation and cognitive gains after bariatric surgery. Psychosom Med. 2015;77(6):688–96. https://doi.org/10.1097/psy.0000000000000125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Netto BD, Bettini SC, Clemente AP, et al. Roux-en-Y gastric bypass decreases pro-inflammatory and thrombotic biomarkers in individuals with extreme obesity. Obes Surg. 2015;25(6):1010–8. https://doi.org/10.1007/s11695-014-1484-7.

    Article  PubMed  Google Scholar 

  70. Chalut-Carpentier A, Pataky Z, Golay A, et al. Involvement of dietary fatty acids in multiple biological and psychological functions, in morbidly obese subjects. Obes Surg. 2015;25(6):1031–8. https://doi.org/10.1007/s11695-014-1471-z.

    Article  PubMed  Google Scholar 

  71. Flores L, Nunez I, Vidal J, et al. Endothelial function in hypertensive obese patients: 1 year after surgically induced weight loss. Obes Surg. 2014;24(9):1581–4. https://doi.org/10.1007/s11695-014-1328-5.

    Article  CAS  PubMed  Google Scholar 

  72. Pallayova M, Steele KE, Magnuson TH, et al. Sleep apnea determines soluble TNF-α receptor 2 response to massive weight loss. Obes Surg. 2011;21(9):1413–23. https://doi.org/10.1007/s11695-011-0359-4.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Agrawal V, Krause KR, Chengelis DL, et al. Relation between degree of weight loss after bariatric surgery and reduction in albuminuria and C-reactive protein. Surg Obes Relat Dis. 2009;5(1):20–6.

    PubMed  Google Scholar 

  74. Torriani M, Oliveira AL, Azevedo DC, et al. Effects of Roux-en-Y gastric bypass surgery on visceral and subcutaneous fat density by computed tomography. Obes Surg. 2014;25(2):381–5. https://doi.org/10.1007/s11695-014-1485-6.

    Article  Google Scholar 

  75. Sparks JA, Halperin F, Karlson JC, et al. Impact of bariatric surgery on patients with rheumatoid arthritis. Arthritis Care Res. 2015;67(12):1619–26. https://doi.org/10.1002/acr.22629.

    Article  CAS  Google Scholar 

  76. Nijhawan S, Richards W, O'Hea MF, et al. Bariatric surgery rapidly improves mitochondrial respiration in morbidly obese patients. Surg Endosc. 2013;27(12):4569–73. https://doi.org/10.1007/s00464-013-3125-y.

    Article  PubMed  Google Scholar 

  77. Ruiz-Tovar J, Oller I, Galindo I, et al. Change in levels of C-reactive protein (CRP) and serum cortisol in morbidly obese patients after laparoscopic sleeve gastrectomy. Obes Surg. 2013;23(6):764–9. https://doi.org/10.1007/s11695-013-0865-7.

    Article  PubMed  Google Scholar 

  78. Woodard GA, Peraza J, Bravo S, et al. One year improvements in cardiovascular risk factors: a comparative trial of laparoscopic Roux-en-Y gastric bypass vs. adjustable gastric banding. Obes Surg. 2010;20(5):578–82.

    PubMed  Google Scholar 

  79. Kelly AS, Ryder JR, Marlatt KL, et al. Changes in inflammation, oxidative stress and adipokines following bariatric surgery among adolescents with severe obesity. Int J Obes (2005). 2016;40(2):275–80. https://doi.org/10.1038/ijo.2015.174.

    Article  CAS  Google Scholar 

  80. Brethauer SA, Heneghan HM, Eldar S, et al. Early effects of gastric bypass on endothelial function, inflammation, and cardiovascular risk in obese patients. Surg Endosc. 2011;25(8):2650–9.

    PubMed  Google Scholar 

  81. Tamboli RA, Hajri T, Jiang A, et al. Reduction in inflammatory gene expression in skeletal muscle from Roux-en-Y gastric bypass patients randomized to omentectomy. PLoS One. 2011;6(12):e28577. https://doi.org/10.1371/journal.pone.0028577.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Ueda Y, Hajri T, Peng D, et al. Reduction of 8-iso-prostaglandin F2α in the first week after Roux-en-Y gastric bypass surgery. Obesity. 2011;19(8):1663–8. https://doi.org/10.1038/oby.2011.58.

    Article  CAS  PubMed  Google Scholar 

  83. Zagorski SM, Papa NN, Chung MH. The effect of weight loss after gastric bypass on C-reactive protein levels. Surg Obes Relat Dis. 2005;1(2):81–5.

    PubMed  Google Scholar 

  84. Huang H, Kasumov T, Gatmaitan P, et al. Gastric bypass surgery reduces plasma ceramide subspecies and improves insulin sensitivity in severely obese patients. Obesity. 2011;19(11):2235–40.

    CAS  PubMed  Google Scholar 

  85. Ramsay MAE. The chronic inflammation of obesity and its effects on surgery and anesthesia. Int Anesthesiol Clin. 2013;51(3):1–12. https://doi.org/10.1097/AIA.0b013e3182981219.

    Article  PubMed  Google Scholar 

  86. Shimizu H, Hatao F, Imamura K, et al. Early effects of sleeve gastrectomy on obesity-related cytokines and bile acid metabolism in morbidly obese Japanese patients. Obes Surg. 2017;27(12):3223–9.

    PubMed  Google Scholar 

  87. Pardina E, Ferrer R, Baena-Fustegueras JA, et al. Only C-reactive protein, but not TNF-alpha or IL6, reflects the improvement in inflammation after bariatric surgery. Obes Surg. 2012;22(1):131–9. https://doi.org/10.1007/s11695-011-0546-3.

    Article  PubMed  Google Scholar 

  88. Vázquez LA, Pazos F, Berrazueta JR, et al. Effects of changes in body weight and insulin resistance on inflammation and endothelial function in morbid obesity after bariatric surgery. J Clin Endocrinol Metab. 2005;90(1):316–22.

    PubMed  Google Scholar 

  89. Pérez-Romero N, Serra A, Granada ML, et al. Effects of two variants of Roux-en-Y gastric bypass on metabolism behaviour: focus on plasma ghrelin concentrations over a 2-year follow-up. Obes Surg. 2010;20(5):600–9.

    PubMed  Google Scholar 

  90. Garrido-Sanchez L, Murri M, Rivas-Becerra J, et al. Bypass of the duodenum improves insulin resistance much more rapidly than sleeve gastrectomy. Surg Obes Relat Dis. 2012;8(2):145–50. https://doi.org/10.1016/j.soard.2011.03.010.

    Article  CAS  PubMed  Google Scholar 

  91. Arismendi E, Rivas E, Agusti A, et al. The systemic inflammome of severe obesity before and after bariatric surgery. PLoS One. 2014;9(9):e107859. https://doi.org/10.1371/journal.pone.0107859.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. De Luis D, Pacheco D, Aller R, et al. Influence of G308A polymorphism of tumor necrosis factor alpha gene on surgical results of biliopancreatic diversion. Obes Surg. 2010;20(2):221–5.

    PubMed  Google Scholar 

  93. Maymó-Masip E, Fernández-Veledo S, España AG, et al. The rise of soluble TWEAK levels in severely obese subjects after bariatric surgery may affect adipocyte-cytokine production induced by TNFα. J Clin Endocrinol Metab. 2013;98(8):E1323–E33. https://doi.org/10.1210/jc.2012-4177.

    Article  CAS  PubMed  Google Scholar 

  94. Parreno Caparros E, Illan Gomez F, Gonzalvez Ortega M, et al. Resistin in morbidly obese patients before and after gastric bypass surgery. Nutr Hosp. 2017;34(5):1333–7. https://doi.org/10.20960/nh.1028.

    Article  PubMed  Google Scholar 

  95. Gómez FI, Ortega MG, Alonso AA, et al. Obesity, endothelial function and inflammation: the effects of weight loss after bariatric surgery. Nutr Hosp. 2016;33(6)

  96. Chen S-B, Lee Y-C, Ser K-H, et al. Serum C-reactive protein and white blood cell count in morbidly obese surgical patients. Obes Surg. 2009;19(4):461–6.

    PubMed  Google Scholar 

  97. Knøsgaard L, Thomsen SB, Støckel M, et al. Circulating sCD36 is associated with unhealthy fat distribution and elevated circulating triglycerides in morbidly obese individuals. Nutr Diabetes. 2014;4:e114. https://doi.org/10.1038/nutd.2014.11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Bueter M, Dubb S, Gill A, et al. Renal cytokines improve early after bariatric surgery. Br J Surg. 2010;97(12):1838–44.

    CAS  PubMed  Google Scholar 

  99. Lammert A, Hasenberg T, Kraupner C, et al. Improved arteriole-to-venule ratio of retinal vessels resulting from bariatric surgery. Obesity (Silver Spring). 2012;20(11):2262–7. https://doi.org/10.1038/oby.2012.122.

    Article  CAS  Google Scholar 

  100. Mallipedhi A, Prior SL, Barry JD, et al. Changes in inflammatory markers after sleeve gastrectomy in patients with impaired glucose homeostasis and type 2 diabetes. Surg Obes Relat Dis. 2014;10(6):1123–8. https://doi.org/10.1016/j.soard.2014.04.019.

    Article  PubMed  Google Scholar 

  101. van de Sande-Lee S, Pereira FR, Cintra DE, Fernandes PT, Cardoso AR, Garlipp CR, et al. Partial reversibility of hypothalamic dysfunction and changes in brain activity after body mass reduction in obese subjects. Diabetes. 20111;60(6):1699–704.

  102. Geloneze S, Geloneze B, Morari J, et al. PGC1α gene Gly482Ser polymorphism predicts improved metabolic, inflammatory and vascular outcomes following bariatric surgery. Int J Obes. 2012;36(3):363–8.

    CAS  Google Scholar 

  103. Boesing F, Moreira EAM, Wilhelm-Filho D, et al. Roux-en-Y bypass gastroplasty: markers of oxidative stress 6 months after surgery. Obes Surg. 2010;20(9):1236–44.

    PubMed  Google Scholar 

  104. Lambert G, de Oliveira Lima MM, Felici A, 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.

    CAS  PubMed  Google Scholar 

  105. Saleh MH, Bertolami MC, Assef JE, et al. Improvement of atherosclerotic markers in non-diabetic patients after bariatric surgery. Obes Surg. 2012;22(11):1701–7. https://doi.org/10.1007/s11695-012-0706-0.

    Article  PubMed  Google Scholar 

  106. de Moura-Grec PG, Yamashita JM, Marsicano JA, et al. Impact of bariatric surgery on oral health conditions: 6-months cohort study. Int Dent J. 2014;64(3):144–9. https://doi.org/10.1111/idj.12090.

    Article  PubMed  Google Scholar 

  107. Sales-Peres SH, de Moura-Grec PG, Yamashita JM, et al. Periodontal status and pathogenic bacteria after gastric bypass: a cohort study. J Clin Periodontol. 2015;42(6):530–6. https://doi.org/10.1111/jcpe.12410.

    Article  CAS  PubMed  Google Scholar 

  108. Oliveira CS, Beserra BTS, Cunha RSG, et al. Impact of Roux-en-Y gastric bypass on lipid and inflammatory profiles. Rev Col Bras Cir. 2015;42(5):305–10. https://doi.org/10.1590/0100-69912015005007.

    Article  Google Scholar 

  109. Iannelli A, Anty R, Schneck AS, et al. Inflammation, insulin resistance, lipid disturbances, anthropometrics, and metabolic syndrome in morbidly obese patients: a case control study comparing laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy. Surgery. 2011;149(3):364–70.

    PubMed  Google Scholar 

  110. Iannelli A, Anty R, Schneck AS, et al. Evolution of low-grade systemic inflammation, insulin resistance, anthropometrics, resting energy expenditure and metabolic syndrome after bariatric surgery: a comparative study between gastric bypass and sleeve gastrectomy. J Visc Surg. 2013;150(4):269–75. https://doi.org/10.1016/j.jviscsurg.2013.08.005.

    Article  CAS  PubMed  Google Scholar 

  111. Richette P, Poitou C, Garnero P, et al. Benefits of massive weight loss on symptoms, systemic inflammation and cartilage turnover in obese patients with knee osteoarthritis. Ann Rheum Dis. 2011;70(1):139–44. https://doi.org/10.1136/ard.2010.134015.

    Article  CAS  PubMed  Google Scholar 

  112. Richette P, Poitou C, Manivet P, et al. Weight loss, xanthine oxidase, and serum urate levels: a prospective longitudinal study of obese patients. Arthritis Care Res (Hoboken). 2016;68(7):1036–42. https://doi.org/10.1002/acr.22798.

    Article  CAS  Google Scholar 

  113. Favre G, Anty R, Canivet C, et al. Determinants associated with the correction of glomerular hyper-filtration one year after bariatric surgery. Surg Obes Relat Dis. 2017;13(10):1760–6. https://doi.org/10.1016/j.soard.2017.07.018.

    Article  PubMed  Google Scholar 

  114. Sans A, Bailly L, Anty R, et al. Baseline anthropometric and metabolic parameters correlate with weight loss in women 1-year after laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2017;27(11):2940–9. https://doi.org/10.1007/s11695-017-2720-8.

    Article  PubMed  Google Scholar 

  115. Tschoner A, Sturm W, Ress C, et al. Effect of weight loss on serum pigment epithelium-derived factor levels. Eur J Clin Investig. 2011;41(9):937–42.

    CAS  Google Scholar 

  116. Ress C, Tschoner A, Engl J, et al. Effect of bariatric surgery on circulating chemerin levels. Eur J Clin Investig. 2010;40(3):277–80.

    CAS  Google Scholar 

  117. Wong AT, Chan DC, Armstrong J, et al. Effect of laparoscopic sleeve gastrectomy on elevated C-reactive protein and atherogenic dyslipidemia in morbidly obese patients. Clin Biochem. 2011;44(4):342–4.

    CAS  PubMed  Google Scholar 

  118. Moschen AR, Molnar C, Enrich B, et al. Adipose and liver expression of interleukin (IL)-1 family members in morbid obesity and effects of weight loss. Mol Med. 2011;17(7–8):840–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Thöni V, Pfister A, Melmer A, et al. Dynamics of bile acid profiles, GLP-1, and FGF19 after laparoscopic gastric banding. J Clin Endocrinol Metab. 2017;102(8):2974–84.

    PubMed  Google Scholar 

  120. Jürets A, Itariu BK, Keindl M, et al. Upregulated TNF expression 1 year after bariatric surgery reflects a cachexia-like state in subcutaneous adipose tissue. Obes Surg. 2017;27(6):1514–23. https://doi.org/10.1007/s11695-016-2477-5.

    Article  PubMed  Google Scholar 

  121. Iaffaldano L, Nardelli C, Pilone V, et al. Laparoscopic adjustable gastric banding reduces subcutaneous adipose tissue and blood inflammation in nondiabetic morbidly obese individuals. Obes Surg. 2014;24(12):2161–8.

    PubMed  Google Scholar 

  122. Campello E, Zabeo E, Radu CM, et al. Dynamics of circulating microparticles in obesity after weight loss. Intern Emerg Med. 2016;11(5):695–702. https://doi.org/10.1007/s11739-016-1397-7.

    Article  PubMed  Google Scholar 

  123. Santilli F, Guagnano MT, Innocenti P, et al. Pentraxin 3 and platelet activation in obese patients after gastric banding. Circ J. 2016;80(2):502–11. https://doi.org/10.1253/circj.CJ-15-0721.

    Article  CAS  PubMed  Google Scholar 

  124. Di Renzo L, Carbonelli M, Bianchi A, et al. Body composition changes after laparoscopic adjustable gastric banding: what is the role of− 174G> C interleukin-6 promoter gene polymorphism in the therapeutic strategy? Int J Obes. 2012;36(3):369–78.

    Google Scholar 

  125. 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 Prev Biomark. 2008;17(6):1401–10.

    CAS  Google Scholar 

  126. Farey JE, Fisher OM, Levert-Mignon AJ, et al. Decreased levels of circulating cancer-associated protein biomarkers following bariatric surgery. Obes Surg. 2017;27(3):578–85. https://doi.org/10.1007/s11695-016-2321-y.

    Article  PubMed  Google Scholar 

  127. Gannagé-Yared M-H, Yaghi C, Habre B, et al. Osteoprotegerin in relation to body weight, lipid parameters insulin sensitivity, adipocytokines, and C-reactive protein in obese and non-obese young individuals: results from both cross-sectional and interventional study. Eur J Endocrinol. 2008;158(3):353–9.

    PubMed  Google Scholar 

  128. Maruna P, Gürlich R, Fried M, et al. Leptin as an acute phase reactant after non-adjustable laparoscopic gastric banding. Obes Surg. 2001;11(5):609–14.

    CAS  PubMed  Google Scholar 

  129. Gjessing HR, Nielsen HJ, Mellgren G, et al. Energy intake, nutritional status and weight reduction in patients one year after laparoscopic sleeve gastrectomy. SpringerPlus. 2013;2:352. https://doi.org/10.1186/2193-1801-2-352.

    Article  PubMed  PubMed Central  Google Scholar 

  130. Nestvold TK, Nielsen EW, Ludviksen JK, et al. Lifestyle changes followed by bariatric surgery lower inflammatory markers and the cardiovascular risk factors C3 and C4. Metab Syndr Relat Disord. 2015;13(1):29–35. https://doi.org/10.1089/met.2014.0099.

    Article  CAS  PubMed  Google Scholar 

  131. Santos J, Salgado P, Santos C, et al. Effect of bariatric surgery on weight loss, inflammation, iron metabolism, and lipid profile. Scand J Surg. 2014;103(1):21–5. https://doi.org/10.1177/1457496913490467.

    Article  CAS  PubMed  Google Scholar 

  132. Yang P-J, Lee W-J, Tseng P-H, et al. Bariatric surgery decreased the serum level of an endotoxin-associated marker: lipopolysaccharide-binding protein. Surg Obes Relat Dis. 2014;10(6):1182–7.

    PubMed  Google Scholar 

  133. Hakeam HA, O’Regan PJ, Salem AM, et al. Impact of laparoscopic sleeve gastrectomy on iron indices: 1 year follow-up. Obes Surg. 2009;19(11):1491–6.

    PubMed  Google Scholar 

  134. Hakeam HA, O’Regan PJ, Salem AM, et al. Inhibition of C-reactive protein in morbidly obese patients after laparoscopic sleeve gastrectomy. Obes Surg. 2009;19(4):456–60.

    PubMed  Google Scholar 

  135. Randell EW, Twells LK, Gregory DM, et al. Pre-operative and post-operative changes in CRP and other biomarkers sensitive to inflammatory status in patients with severe obesity undergoing laparoscopic sleeve gastrectomy. Clin Biochem. 2018;52:13–9.

    CAS  PubMed  Google Scholar 

  136. Chung MY, Hong SJ, Lee JY. The influence of obesity on postoperative inflammatory cytokine levels. J Int Med Res. 2011;39(6):2370–8. https://doi.org/10.1177/147323001103900637.

    Article  CAS  PubMed  Google Scholar 

  137. Park S, Kim YJ, C-y C, et al. Bariatric surgery can reduce albuminuria in patients with severe obesity and normal kidney function by reducing systemic inflammation. Obes Surg. 2018;28(3):831–7.

    PubMed  Google Scholar 

  138. Gesquiere I, Foulon V, Augustijns P, et al. Micronutrient intake, from diet and supplements, and association with status markers in pre- and post-RYGB patients. Clin Nutr (Edinburgh, Scotland). 2017;36(4):1175–81. https://doi.org/10.1016/j.clnu.2016.08.009.

    Article  CAS  Google Scholar 

  139. Werling M, Vincent RP, Cross GF, et al. Enhanced fasting and post-prandial plasma bile acid responses after Roux-en-Y gastric bypass surgery. Scand J Gastroenterol. 2013;48(11):1257–64. https://doi.org/10.3109/00365521.2013.833647.

    Article  PubMed  Google Scholar 

  140. Johansson HE, Wahlen A, Aldenback E, et al. Platelet counts and liver enzymes after gastric bypass surgery. Obes Surg. 2017;28:1526–31. https://doi.org/10.1007/s11695-017-3035-5.

    Article  PubMed Central  Google Scholar 

  141. Montecucco F, Lenglet S, Quercioli A, et al. Gastric bypass in morbid obese patients is associated with reduction in adipose tissue inflammation via N-oleoylethanolamide (OEA)-mediated pathways. Thromb Haemost. 2015;113(4):838–50. https://doi.org/10.1160/th14-06-0506.

    Article  PubMed  Google Scholar 

  142. Galanakis CG, Daskalakis M, Manios A, et al. Computed tomography-based assessment of abdominal adiposity changes and their impact on metabolic alterations following bariatric surgery. World J Surg. 2015;39(2):417–23. https://doi.org/10.1007/s00268-014-2826-2.

    Article  PubMed  Google Scholar 

  143. Rao SR. Inflammatory markers and bariatric surgery: a meta-analysis. Inflamm Res. 2012;61(8):789–807.

    CAS  PubMed  Google Scholar 

  144. Heilbronn L, Noakes M, Clifton P. Energy restriction and weight loss on very-low-fat diets reduce C-reactive protein concentrations in obese, healthy women. Arterioscler Thromb Vasc Biol. 2001;21(6):968–70.

    CAS  PubMed  Google Scholar 

  145. Bastard J-P, Jardel C, Bruckert E, et al. Elevated levels of interleukin 6 are reduced in serum and subcutaneous adipose tissue of obese women after weight loss. J Clin Endocrinol Metab. 2000;85(9):3338–42.

    CAS  PubMed  Google Scholar 

  146. Bueno NB, de Melo ISV, de Oliveira SL, et al. Very-low-carbohydrate ketogenic diet v. low-fat diet for long-term weight loss: a meta-analysis of randomised controlled trials. Br J Nutr. 2013;110(7):1178–87.

    CAS  PubMed  Google Scholar 

  147. Gill JM, Malkova D. Physical activity, fitness and cardiovascular disease risk in adults: interactions with insulin resistance and obesity. Clin Sci. 2006;110(4):409–25.

    CAS  Google Scholar 

  148. Jung DY, Ko HJ, Lichtman EI, et al. Short-term weight loss attenuates local tissue inflammation and improves insulin sensitivity without affecting adipose inflammation in obese mice. Am J Physiol Endocrinol Metab. 2013;304(9):E964–E76.

    CAS  PubMed  PubMed Central  Google Scholar 

  149. Cancello R, Clement K. Is obesity an inflammatory illness? Role of low-grade inflammation and macrophage infiltration in human white adipose tissue. BJOG Int J Obstet Gynaecol. 2006;113(10):1141–7.

    CAS  Google Scholar 

  150. Howe LR, Subbaramaiah K, Hudis CA, Dannenberg AJ. Molecular pathways: adipose inflammation as a mediator of obesity-associated cancer. Clin Cancer Res. 2013;19(22):6074–83.

    CAS  PubMed  PubMed Central  Google Scholar 

  151. Franceschi C, Campisi J. Chronic inflammation (inflammaging) and its potential contribution to age-associated diseases. J Gerontol Ser A Biomed Sci Med Sci. 2014;69(Suppl_1):S4–9.

    Google Scholar 

  152. Rosenblat JD, Cha DS, Mansur RB, et al. Inflamed moods: a review of the interactions between inflammation and mood disorders. Prog Neuro-Psychopharmacol Biol Psychiatry. 2014;53:23–34.

    CAS  Google Scholar 

  153. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352(16):1685–95.

    CAS  PubMed  Google Scholar 

  154. Amor S, Puentes F, Baker D, et al. Inflammation in neurodegenerative diseases. Immunology. 2010;129(2):154–69.

    CAS  PubMed  PubMed Central  Google Scholar 

  155. Mantovani A, Allavena P, Sica A, et al. Cancer-related inflammation. Nature. 2008;454(7203):436–44.

    CAS  PubMed  Google Scholar 

  156. Papi A, Bellettato CM, Braccioni F, et al. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am J Respir Crit Care Med. 2006;173(10):1114–21.

    PubMed  Google Scholar 

  157. Savoia C, Schiffrin EL. Inflammation in hypertension. Curr Opin Nephrol Hypertens. 2006;15(2):152–8.

    CAS  PubMed  Google Scholar 

  158. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115(5):1111–9.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shahab Alizadeh.

Ethics declarations

Ethical issues (including plagiarism, misconduct, data fabrication, falsification, double publication or submission, redundancy) have been completely observed by the authors.

Conflict of Interest

All authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Askarpour, M., Khani, D., Sheikhi, A. et al. Effect of Bariatric Surgery on Serum Inflammatory Factors of Obese Patients: a Systematic Review and Meta-Analysis. OBES SURG 29, 2631–2647 (2019). https://doi.org/10.1007/s11695-019-03926-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11695-019-03926-0

Keywords

Navigation