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Early Effects of Sleeve Gastrectomy on Obesity-Related Cytokines and Bile Acid Metabolism in Morbidly Obese Japanese Patients

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Abstract

Background

Laparoscopic sleeve gastrectomy (LSG) has wide-ranging positive effects on adipocytokine metabolism, bile acid profile, and chronic low-grade inflammation related to obesity. However, the early temporal changes in these markers following LSG have not been well investigated. This study aimed to evaluate the early effects of LSG on adipocytokines, bile acid profile, and inflammatory markers.

Methods

This was a nonrandomized prospective study examining morbidly obese Japanese patients undergoing LSG. Serial measurements of leptin, adiponectin, bile acids, fibroblast growth factor (FGF)-19, and inflammatory markers were performed preoperatively and 1 and 6 months after LSG.

Results

The study included ten patients (five females) with a mean age of 48.8 years and BMI 40.9 kg/m2. At baseline, 90% of the patients had T2DM, 70% had dyslipidemia, and 90% had hypertension. Patients lost 5.1 kg/m2 BMI at 1 month and 10.1 kg/m2 BMI at 6 months. The leptin levels sharply decreased, and FGF-19 increased significantly as early as 1 month postoperatively. Adiponectin levels showed an increasing trend at 1 month and a significant increase at 6 months. A significant decrease in high-sensitivity CRP and plasminogen activator inhibitor-1 was observed at 6 months. No significant changes were observed in interleukin (IL)-6, IL-8, tumor necrosis factor-α, serum amyloid A protein, or monocyte chemotactic protein-1 throughout the study.

Conclusions

LSG improved the secretion of adipocytokines, increased FGF-19 secretion soon after surgery, and slowly ameliorated inflammation related to obesity through significant weight loss.

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References

  1. Adami GF, Gradaschi R, Andraghetti G, et al. Serum leptin and adiponectin concentration in type 2 diabetes patients in the short and long term following biliopancreatic diversion. Obes Surg. 2016;26(10):2442–8.

    Article  PubMed  Google Scholar 

  2. Butner KL, Nickols-Richardson SM, Clark SF, et al. A review of weight loss following Roux-en-Y gastric bypass vs restrictive bariatric surgery: impact on adiponectin and insulin. Obes Surg. 2010;20(5):559–68.

    Article  PubMed  Google Scholar 

  3. Herder C, Peltonen M, Svensson PA, et al. Adiponectin and bariatric surgery: associations with diabetes and cardiovascular disease in the Swedish Obese Subjects Study. Diabetes Care. 2014;37(5):1401–9.

    Article  CAS  PubMed  Google Scholar 

  4. Kopp HP, Krzyzanowska K, Mohlig M, et al. Effects of marked weight loss on plasma levels of adiponectin, markers of chronic subclinical inflammation and insulin resistance in morbidly obese women. Int J Obes. 2005;29(7):766–71.

    Article  CAS  Google Scholar 

  5. Woelnerhanssen B, Peterli R, Steinert RE, et al. Effects of postbariatric surgery weight loss on adipokines and metabolic parameters: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy—a prospective randomized trial. Surgery for Obesity and Related Diseases: Official Journal of the American Society for Bariatric Surgery. 2011;7(5):561–8.

    Article  Google Scholar 

  6. Freeman DJ, Norrie J, Caslake MJ, et al. C-reactive protein is an independent predictor of risk for the development of diabetes in the West of Scotland Coronary Prevention Study. Diabetes. 2002;51(5):1596–600.

    Article  CAS  PubMed  Google Scholar 

  7. Kaptoge S, Di Angelantonio E, Pennells L, et al. C-reactive protein, fibrinogen, and cardiovascular disease prediction. N Engl J med. 2012;367(14):1310–20.

    Article  PubMed  Google Scholar 

  8. Ghigliotti G, Barisione C, Garibaldi S, et al. Adipose tissue immune response: novel triggers and consequences for chronic inflammatory conditions. Inflammation. 2014;37(4):1337–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cottam DR, Mattar SG, Barinas-Mitchell E, et al. The chronic inflammatory hypothesis for the morbidity associated with morbid obesity: implications and effects of weight loss. Obes Surg. 2004;14(5):589–600.

    Article  PubMed  Google Scholar 

  10. Kohli R, Seeley RJ. Diabetes: the search for mechanisms underlying bariatric surgery. Nat rev Endocrinol. 2013;9(10):572–4.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Dutia R, Embrey M, O’Brien CS, et al. Temporal changes in bile acid levels and 12alpha-hydroxylation after Roux-en-Y gastric bypass surgery in type 2 diabetes. Int J Obes. 2015;39(5):806–13.

    Article  CAS  Google Scholar 

  12. Gerhard GS, Styer AM, Wood GC, et al. A role for fibroblast growth factor 19 and bile acids in diabetes remission after Roux-en-Y gastric bypass. Diabetes Care. 2013;36(7):1859–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 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.

    Article  PubMed  Google Scholar 

  14. Gumbau V, Bruna M, Canelles E, et al. A prospective study on inflammatory parameters in obese patients after sleeve gastrectomy. Obes Surg. 2014;24(6):903–8.

    Article  PubMed  Google Scholar 

  15. Umemura A, Sasaki A, Nitta H, et al. Effects of changes in adipocyte hormones and visceral adipose tissue and the reduction of obesity-related comorbidities after laparoscopic sleeve gastrectomy in Japanese patients with severe obesity. Endocr J. 2014;61(4):381–91.

    Article  CAS  PubMed  Google Scholar 

  16. Lihn AS, Pedersen SB, Richelsen B. Adiponectin: action, regulation and association to insulin sensitivity. Obesity Reviews: an Official Journal of the International Association for the Study of Obesity. 2005;6(1):13–21.

    Article  CAS  Google Scholar 

  17. Kwon H, Pessin JE. Adipokines mediate inflammation and insulin resistance. Front Endocrinol. 2013;4:71.

    Article  Google Scholar 

  18. Hotta K, Funahashi T, Bodkin NL, et al. Circulating concentrations of the adipocyte protein adiponectin are decreased in parallel with reduced insulin sensitivity during the progression to type 2 diabetes in rhesus monkeys. Diabetes. 2001;50(5):1126–33.

    Article  CAS  PubMed  Google Scholar 

  19. Malin SK, Bena J, Abood B, et al. Attenuated improvements in adiponectin and fat loss characterize type 2 diabetes non-remission status after bariatric surgery. Diabetes Obes Metab. 2014;16(12):1230–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Al-Suhaimi EA, Shehzad A. Leptin, resistin and visfatin: the missing link between endocrine metabolic disorders and immunity. Eur J med res. 2013;18:12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Modica S, Gadaleta RM, Moschetta A. Deciphering the nuclear bile acid receptor FXR paradigm. Nucl Recept Signal. 2010;8:e005.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Tomlinson E, Fu L, John L, et al. Transgenic mice expressing human fibroblast growth factor-19 display increased metabolic rate and decreased adiposity. Endocrinology. 2002;143(5):1741–7.

    Article  CAS  PubMed  Google Scholar 

  23. Kir S, Beddow SA, Samuel VT, et al. FGF19 as a postprandial, insulin-independent activator of hepatic protein and glycogen synthesis. Science. 2011;331(6024):1621–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ryan KK, Tremaroli V, Clemmensen C, et al. FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature. 2014;509(7499):183–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Jansen PL, van Werven J, Aarts E, et al. Alterations of hormonally active fibroblast growth factors after Roux-en-Y gastric bypass surgery. Dig dis. 2011;29(1):48–51.

    Article  PubMed  Google Scholar 

  26. Patti ME, Houten SM, Bianco AC, et al. Serum bile acids are higher in humans with prior gastric bypass: potential contribution to improved glucose and lipid metabolism. Obesity (Silver Spring). 2009;17(9):1671–7.

    Article  CAS  Google Scholar 

  27. Pournaras DJ, Glicksman C, Vincent RP, et al. The role of bile after Roux-en-Y gastric bypass in promoting weight loss and improving glycaemic control. Endocrinology. 2012;153(8):3613–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sachdev S, Wang Q, Billington C, et al. FGF 19 and bile acids increase following Roux-en-Y gastric bypass but not after medical management in patients with type 2 diabetes. Obes Surg. 2016;26(5):957–65.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Belgaumkar AP, Vincent RP, Carswell KA, et al. Changes in bile acid profile after laparoscopic sleeve gastrectomy are associated with improvements in metabolic profile and fatty liver disease. Obes Surg. 2016;26(6):1195–202.

    Article  PubMed  Google Scholar 

  30. Haluzikova D, Lacinova Z, Kavalkova P, et al. Laparoscopic sleeve gastrectomy differentially affects serum concentrations of FGF-19 and FGF-21 in morbidly obese subjects. Obesity (Silver Spring). 2013;21(7):1335–42.

    Article  CAS  Google Scholar 

  31. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu rev Immunol. 2011;29:415–45.

    Article  CAS  PubMed  Google Scholar 

  32. Saltiel AR, Olefsky JM. Inflammatory mechanisms linking obesity and metabolic disease. J Clin Invest. 2017;127(1):1–4.

    Article  PubMed  Google Scholar 

  33. 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.

    Article  PubMed  Google Scholar 

  34. Ryan AS, Nicklas BJ. Reductions in plasma cytokine levels with weight loss improve insulin sensitivity in overweight and obese postmenopausal women. Diabetes Care. 2004;27(7):1699–705.

    Article  PubMed  Google Scholar 

  35. Schernthaner GH, Kopp HP, Kriwanek S, et al. Effect of massive weight loss induced by bariatric surgery on serum levels of interleukin-18 and monocyte-chemoattractant-protein-1 in morbid obesity. Obes Surg. 2006;16(6):709–15.

    Article  PubMed  Google Scholar 

  36. Poitou C, Coupaye M, Laaban JP, et al. Serum amyloid A and obstructive sleep apnea syndrome before and after surgically-induced weight loss in morbidly obese subjects. Obes Surg. 2006;16(11):1475–81.

    Article  PubMed  Google Scholar 

  37. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J med. 1999;340(6):448–54.

    Article  CAS  PubMed  Google Scholar 

  38. 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. Surgery for Obesity and Related Diseases: Official Journal of the American Society for Bariatric Surgery. 2014;10(6):1123–8.

    Article  Google Scholar 

  39. Ziccardi P, Nappo F, Giugliano G, et al. Reduction of inflammatory cytokine concentrations and improvement of endothelial functions in obese women after weight loss over one year. Circulation. 2002;105(7):804–9.

    Article  CAS  PubMed  Google Scholar 

  40. Lindegaard KK, Jorgensen NB, Just R, et al. Effects of Roux-en-Y gastric bypass on fasting and postprandial inflammation-related parameters in obese subjects with normal glucose tolerance and in obese subjects with type 2 diabetes. Diabetology & Metabolic Syndrome. 2015;7:12.

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Viana EC, Araujo-Dasilio KL, Miguel GP, et al. Gastric bypass and sleeve gastrectomy: the same impact on IL-6 and TNF-alpha. Prospective clinical trial. Obes Surg. 2013;23(8):1252–61.

    Article  PubMed  Google Scholar 

  43. Boekholdt SM, Peters RJ, Hack CE, et al. IL-8 plasma concentrations and the risk of future coronary artery disease in apparently healthy men and women: the EPIC-Norfolk prospective population study. Arterioscler Thromb Vasc Biol. 2004;24(8):1503–8.

    Article  CAS  PubMed  Google Scholar 

  44. Bruun JM, Pedersen SB, Richelsen B. Regulation of interleukin 8 production and gene expression in human adipose tissue in vitro. J Clin Endocrinol Metab. 2001;86(3):1267–73.

    CAS  PubMed  Google Scholar 

  45. Moreau M, Brocheriou I, Petit L, et al. Interleukin-8 mediates downregulation of tissue inhibitor of metalloproteinase-1 expression in cholesterol-loaded human macrophages: relevance to stability of atherosclerotic plaque. Circulation. 1999;99(3):420–6.

    Article  CAS  PubMed  Google Scholar 

  46. Bruun JM, Pedersen SB, Kristensen K, et al. Opposite regulation of interleukin-8 and tumor necrosis factor-alpha by weight loss. Obes res. 2002;10(6):499–506.

    Article  CAS  PubMed  Google Scholar 

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Author information

Authors and Affiliations

  1. Department of Surgery, Tokyo Metropolitan Tama Medical Center, 2-8-29, Musashidai, Fuchu, Tokyo, Japan

    Hideharu Shimizu, Fumihiko Hatao, Kazuhiro Imamura & Kijuro Takanishi

  2. Department of Endocrinology, Tokyo Metropolitan Tama Medical Center, Fuchu, Tokyo, 183-8524, Japan

    Motoyoshi Tsujino

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  1. Hideharu Shimizu
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  2. Fumihiko Hatao
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  3. Kazuhiro Imamura
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  5. Motoyoshi Tsujino
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Correspondence to Hideharu Shimizu.

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Conflict of Interest

The authors have no conflicts of interest or financial ties to disclose.

Human and Animal Rights and Informed Consent

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

Funding

This research was supported by the Clinical Research Fund (H260502002) of Tokyo Metropolitan government.

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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 27, 3223–3229 (2017). https://doi.org/10.1007/s11695-017-2756-9

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  • DOI: https://doi.org/10.1007/s11695-017-2756-9

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