Abstract
Objective
Bariatric surgery (BS) improves glycemic control in type 2 diabetes; however, some patients show insufficient improvement. Understanding the pathophysiology of type 2 diabetes in obese patients can facilitate appropriate treatment for type 2 diabetes after BS. The homeostatic model assessment (HOMA) 2 enables the calculation of the values from C-peptide data and evaluation of insulin users. We aimed to evaluate the pathophysiology of type 2 diabetes using pre- and postoperative parameters and HOMA2 in obese patients who underwent BS.
Methods
We retrospectively reviewed data from 45 obese patients with type 2 diabetes who underwent BS. They were followed-up for 12 months. The relationship between the HOMA2 score and complete remission (CR) of type 2 diabetes after BS was analyzed. Patients with and without CR were assigned to the CR and non-CR groups, respectively. Multiple regression analysis was used to identify factors associated with improvement in type 2 diabetes after BS.
Results
BS significantly improved body weight and glucose metabolism. The preoperative glycosylated hemoglobin A1c level and insulin secretion (HOMA2-%B) significantly differed between the CR and non-CR groups. Postoperative weight reduction and improved insulin sensitivity correlated significantly with CR; multiple regression showed that the preoperative HOMA 2-%B independently predicted CR of type 2 diabetes after BS.
Conclusion
Preoperative insulin secretion, improvement in insulin sensitivity, and weight reduction after BS are related to CR of type 2 diabetes after BS. The results better reveal the pathophysiology of and treatment for type 2 diabetes in obese patients who undergo BS.
Similar content being viewed by others
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Schauer PR, Kashyap SR, Wolski K, Brethauer SA, Kirwan JP, Pothier CE, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med. 2012;366:1567–76.
Khorgami Z, Shoar S, Saber AA, Howard CA, Danaei G, Sclabas GM. Outcomes of bariatric surgery versus medical management for type 2 diabetes mellitus: a meta-analysis of randomized controlled trials. Obes Surg. 2019;29:964–74.
Lee MH, Lee WJ, Chong K, Chen JC, Ser KH, Lee YC, et al. Predictors of long-term diabetes remission after metabolic surgery. J Gastrointest Surg. 2015;19:1015–21.
Rubino F, Nathan DM, Eckel RH, Schauer PR, Alberti KG, Zimmet PZ, et al. Metabolic surgery in the treatment algorithm for type 2 diabetes: a joint statement by international diabetes organizations. Diabetes Care. 2016;39:861–77.
Li YX, Fang DH, Liu TX. Laparoscopic sleeve gastrectomy combined with single-anastomosis duodenal-jejunal bypass in the treatment of type 2 diabetes mellitus of patients with body mass index higher than 27.5 kg/m2 but lower than 32.5 kg/m2. Medicine (Baltimore). 2018;97:e11537.
Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Tumer RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–9.
Levy JC, Matthews DR, Hermans MP. Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care. 1998;21:2191–2.
Song YS, Hwang YC, Ahn HY, Park CY. Comparison of the usefulness of the updated Homeostasis model Assessment (HOMA2) with the original HOMA1 in the prediction of type 2 diabetes mellitus in Koreans. Diabetes Metab J. 2016;40:318–25.
Auguet T, Terra X, Hernández M, Sabench F, Porras JA, Orellana-Gavaldà JM, et al. Clinical and adipocytokine changes after bariatric surgery in morbidly obese women. Obesity. 2014;22:188–94.
Mathieu C, Del Prato S, Botros FT, Thieu VT, Pavo I, Jia N, et al. Effect of once weekly dulaglutide by baseline beta-cell function in people with type 2 diabetes in the AWARD programme. Diabetes Obes Metab. 2018;20:2023–8.
Saiki A, Yamaguchi T, Tanaka S, Sasaki A, Naitoh T, Seto Y, et al. Background characteristics and postoperative outcomes of insufficient weight loss after laparoscopic sleeve gastrectomy in Japanese patients. Ann Gastroenterol Surg. 2019;3:638–47.
Fellici AC, Lambert G, Lima MM, Pareja JC, Rodovalho S, Chaim EA, et al. Surgical treatment of type 2 diabetes in subjects with mild obesity: mechanisms underlying metabolic improvements. Obes Surg. 2015;25:36–44.
Benaiges D, Flores Le-Reox JA, Pedro-Botet J, Chillarón JJ, Renard M, Parri A, et al. Sleeve gastrectomy and Roux-en-Y gastric bypass are equally effective in correcting insulin resistance. Int J Surg. 2013;11:309–13.
Zhu Y, Sun Z, Du Y, Xu G, Gong K, Zhu B, et al. Evaluation of insulin resistance improvement after laparoscopic sleeve gastrectomy or gastric bypass surgery with HOMA-IR. Biosci Trends. 2017;11:675–81.
Liu T, Zhong MW, Liu Y, Sun D, Wei M, Huang X, et al. Diabetes recurrence after metabolic surgeries correlates with re-impaired insulin sensitivity rather than beta-cell function. World J Gastroenterol. 2017;23:3468–79.
Yan YX, Wang GF, Xu N, Wang FL. Correlation between postoperative weight loss and diabetes mellitus remission: a meta-analysis. Obes surg. 2014;24:1862–9.
Park JY, Kim YJ. Prediction of diabetes remission in morbidly obese patients after Roux-en-Y gastric bypass. Obes Surg. 2016;26:749–56.
Villarreal-Calderón JR, Cuéllar RX, Ramos-González MR, Rubio-Infante N, Castillo EC, Elizondo-Montemayor L, et al. Interplay between the adaptive immune system and insulin resistance in weight loss induced by bariatric surgery. Oxid Med Cell Longev. 2019;2019:3940739.
Goktas Z, Moustaid-Moussa N, Shen CL, Boylan M, Mo H, Wang S. Effects of bariatric surgery on adipokine-induced inflammation and insulin resistance. Front Endocrinol (Lausanne). 2013;4:69.
Pèrez-Pevida B, Escalada J, Miras AD, Frühbeck G. Mechanisms underlying type 2 diabetes remission after metabolic surgery. Front Endocrinol (Lausanne). 2019;10:641.
Saiki A, Oyama T, Endo K, Ebisuno M, Ohira M, Koide N, et al. Preheparin serum lipoprotein lipase mass might be a biomarker of metabolic syndrome. Diabetes Res Clin Pract. 2007;76:93–101.
Ohira M, Yamaguchi T, Saiki A, Nakamura S, Tanaka S, Oka R, et al. Laparoscopic sleeve gastrectomy significantly increases serum lipoprotein lipase level in patients with obesity. Obes Facts. 2019;12:357–68.
Samaras K, Viardot A, Botelho NK, Jenkins A, Lord RV. Immune cell-mediated inflammation and the early improvements in glucose metabolism after gastric banding surgery. Diabetologia. 2013;56:2564–72.
Zagorski SM, Papa NN, Chung MH. The effect of weight loss after gastric bypass on C-reactive protein levels. Surg Obes Relat Dis. 2005;1:81–5.
Patti ME, Houten SM, Bianco AC, Bernier R, Larsen PR, Holst JJ, 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;17:1671–7.
Shapiro H, Kolodziejczyk AA, Halstuch D, Elinav E. Bile acids in glucose metabolism in health and disease. J Exp Med. 2018;215:383–96.
Genske F, Kühn JP, Pietzner M, Homuth G, Rathmann W, Grabe HJ, et al. Abdominal fat deposits determined by magnetic resonance imaging in relation to leptin and vaspin levels as well as insulin resistance in the general adult population. Int J Obes. 2018;42:183–9.
Thamer C, Machann J, Staiger H, Müssig K, Schwenzer N, Ludescher B, et al. Interscapular fat is strongly associated with insulin resistance. J Clin Endocrinol Metab. 2010;95:4736–42.
Saito T, Murata M, Otani T, Tamemoto H, Kawakami M, Ishikawa SE. Association of subcutaneous and visceral fat mass with serum concentrations of adipokines in subjects with type 2 diabetes mellitus. Endocr J. 2012;59:39–45.
Lee WJ, Chong K, Ser KH, Chen JC, Lee YC, Chen SC, et al. C-peptide predicts the remission of type 2 diabetes after bariatric surgery. Obes Surg. 2012;22(2):293–8.
Dixon JB, Chuang LM, Chong K, Chen SC, Lambert GW, Straznicky NE, et al. Predicting the glycemic response to gastric bypass surgery in patients with type 2 diabetes. Diabetes Care. 2013;36:20–6.
Wang GF, Yan YX, Xu N, Yin D, Hui Y, Zhang JP, et al. Predictive factors of type 2 diabetes mellitus remission following bariatric surgery: a meta-analysis. Obes Surg. 2015;25:199–208.
Chong K, Ikramuddin S, Lee WJ, Billington CJ, Bantle JP, Wang Q, et al. National differences in remission of type 2 diabetes mellitus after Roux-en-Y gastric bypass surgery-subgroup analysis of 2 year results of the diabetes surgery study comparing Taiwanese with Americans with mild obesity (BMI 30–35 kg/m2). Obes Surg. 2017;27:1189–95.
Yan H, Tang L, Chen T, Kral JG, Jiang L, Li Y, et al. Defining and predicting complete remission of type 2 diabetes: a short-term efficacy study of open gastric bypass. Obes Facts. 2013;6:176–84.
Wentworth JM, Playfair J, Laurie C, Brown WA, Burton P, Shaw JE, et al. Gastric band surgery leads to improve insulin secretion in overweight people with type 2 diabetes. Obes Surg. 2015;25:2400–7.
Dutia R, Brakoniecki K, Bunker P, Paultre F, Homel P, Carpentier AC, et al. Limited recovery of beta-cell function after gastric bypass despite clinical diabetes remission. Diabetes. 2014;63:1214–23.
Brethauer SA, Kim J, el Chaar M, Papasavas P, Eisenberg D, Rogers A, et al. Standardized outcomes reporting in metabolic and bariatric surgery. Surg Obes Relat Dis. 2015;11:489–506.
Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care. 2004;27:1487–95.
Acknowledgements
The authors are grateful to Dr. Daiji Nagayama (Nagayama Clinic, Oyama-city, Tochigi, Japan) for his assistance with statistical analysis and to Sayaka Tsuji (Center for Diabetes, Endocrinology and Metabolism, Toho University Sakura Medical Center, Sakura-City, Chiba, Japan), a coordinator, for her assistance with patient care. The authors are also grateful to the radiologists who measured the fat mass in this study.
Funding
This study did not receive any funding.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. MO contributed to the research concept and design, collection and/or assembly of data, data analysis, and writing of the article. YW, TY, AS, SN, ST, NS, TN, and TO contributed to data collection and/or collation. IT contributed to the interpretation of the results of data analysis and to the critical revision of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no competing interests.
Research involving human participants and/or animals
All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional) and/or with the Helsinki Declaration of 1964 and later versions. The protocol of the study was approved by the Ethics Committee of Toho University Sakura Medical Center (approval date; 28 November 2018, approval No.; S18061).
Informed consent
Although this was a retrospective study, patients were individually explained the issues relating to the use and release of the study data before the operation. Written consent was obtained in each case.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Ohira, M., Watanabe, Y., Yamaguchi, T. et al. Determinants of type 2 diabetes remission after bariatric surgery in obese Japanese patients: a retrospective cohort study. Diabetol Int 12, 379–388 (2021). https://doi.org/10.1007/s13340-021-00493-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13340-021-00493-7