Positive Changes in Body Composition and Profiles of Individuals with Diabetes 3 Years Following Laparoscopic Sleeve Gastrectomy in Japanese Patients with Obesity
Abstract
:1. Introduction
2. Materials and Methods
2.1. Research Design and Participants
2.2. Surgery
2.3. Collection of Measurement Parameters and Blood Data
2.4. Analysis of Body Weight and Body Composition
2.5. Statistical Analyses
3. Results
3.1. Clinical Characteristics of Patients and Changes in BW and BMI Following LSG
3.2. Changes in Plasma Metabolic Parameters and Antidiabetic, Antihypertensive, and Lipid-Lowering Medications Use Following LSG
3.3. Time-Course Changes of FM and, % FM After LSG
3.4. Changes in Muscle Mass and the Ratio of Extra Cellular Fluid and Bone Mineral Content After LSG
3.5. Relationship Between Alterations in Body Compositions and Variations in BW and Glycemic Metabolic Parameters 3 Years Post-LSG
3.6. 3 Years Post-LSG, Multiple Regression Analyses Regarding Changes in Body Weight, FPG, and HbA1c
4. Discussion
5. Limitations
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Brown, O.I.; Drozd, M.; McGowan, H.; Giannoudi, M.; Conning-Rowland, M.; Gierula, J.; Straw, S.; Wheatcroft, S.B.; Bridge, K.; Roberts, L.D.; et al. Relationship among diabetes, obesity, and cardiovascular disease phenotypes: A UK Biobank cohort study. Diabetes Care 2023, 46, 1531–1540. [Google Scholar] [CrossRef] [PubMed]
- Yoo, H.J. Body Mass Index and Mortality. J. Obes. Metab. Syndr. 2017, 26, 3–9. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Copeland, W.K.; Vedanthan, R.; Grant, E.; Lee, J.E.; Gu, D.; Gupta, P.C.; Ramadas, K.; Inoue, M.; Tsugane, S.; et al. Association between body mass index and cardiovascular disease mortality in east Asians and South Asians: Pooled analysis of prospective data from the Asia Cohort Consortium. BMJ 2013, 347, f5446. [Google Scholar] [CrossRef] [PubMed]
- Boutari, C.; DeMarsilis, A.; Mantzoros, C.S. Obesity and diabetes. Diabetes Res. Clin. Pract. 2023, 202, 110773. [Google Scholar] [CrossRef] [PubMed]
- Shoar, S.; Mahmoudzadeh, H.; Naderan, M.; Bagheri-Hariri, S.; Wong, C.; Parizi, A.S.; Shoar, N. Long-Term Outcome of Bariatric Surgery in Morbidly Obese Adolescents: A Systematic Review and Meta-Analysis of 950 Patients with a Minimum of 3 years Follow-Up. Obes. Surg. 2017, 27, 3110–3117. [Google Scholar] [CrossRef]
- Svanevik, M.; Lorentzen, J.; Borgeraas, H.; Sandbu, R.; Seip, B.; Medhus, A.W.; Hertel, J.K.; Kolotkin, R.L.; Småstuen, M.C.; Hofsø, D.; et al. Patient-reported outcomes, weight loss, and remission of type 2 diabetes 3 years after gastric bypass and sleeve gastrectomy (Oseberg): A single-centre, randomised controlled trial. Lancet Diabetes Endocrinol. 2023, 11, 555–566. [Google Scholar] [CrossRef]
- Seki, Y.; Kasama, K.; Kikkawa, E.; Yokoyama, R.; Nabekura, T.; Sano, A.; Amiki, M.; Kurokawa, Y. Five-year outcomes of laparoscopic sleeve gastrectomy in Japanese patients with Class I obesity. Obes. Surg. 2020, 30, 4366–4374. [Google Scholar] [CrossRef]
- Boza, C.; Daroch, D.; Barros, D.; León, F.; Funke, R.; Crovari, F. Long-term outcomes of laparoscopic sleeve gastrectomy as a primary bariatric procedure. Surg. Obes. Relat. Dis. 2014, 10, 1129–1133. [Google Scholar] [CrossRef]
- Wajchenberg, B.L. Subcutaneous and visceral adipose tissue: Their relation to the metabolic syndrome. Endocr. Rev. 2000, 21, 697–738. [Google Scholar] [CrossRef]
- Hamasaki, H.; Kawashima, Y.; Adachi, H.; Moriyama, S.; Katsuyama, H.; Sako, A.; Yanai, H. Associations between lower extremity muscle mass and metabolic parameters related to obesity in Japanese obese patients with type 2 diabetes. PeerJ 2015, 3, e942. [Google Scholar] [CrossRef]
- Wannamethee, S.G.; Atkins, J.L. Muscle loss and obesity: The health implications of sarcopenia and sarcopenic obesity. Proc. Nutr. Soc. 2015, 74, 405–412. [Google Scholar] [CrossRef] [PubMed]
- Goodpaster, B.H.; Thaete, F.L.; Simoneau, J.A.; Kelley, D.E. Subcutaneous abdominal fat and thigh muscle composition predict insulin sensitivity independently of visceral fat. Diabetes 1997, 46, 1579–1585. [Google Scholar] [CrossRef] [PubMed]
- Yang, J. Enhanced skeletal muscle for effective glucose homeostasis. Prog. Mol. Biol. Transl. Sci. 2014, 121, 133–163. [Google Scholar] [PubMed]
- Xiao, J.; Purcell, S.A.; Prado, C.M.; Gonzalez, M.C. Fat mass to fat-free mass ratio reference values from NHANES III using bioelectrical impedance analysis. Clin. Nutr. 2018, 37, 2284–2287. [Google Scholar] [CrossRef] [PubMed]
- Buffa, R.; Mereu, E.; Comandini, O.; Ibanez, M.E.; Marini, E. Bioelectrical impedance vector analysis (BIVA) for the assessment of two-compartment body composition. Eur. J. Clin. Nutr. 2014, 68, 1234–1240. [Google Scholar] [CrossRef]
- Widen, E.M.; Strain, G.; King, W.C.; Yu, W.; Lin, S.; Goodpaster, B.; Thornton, J.; Courcoulas, A.; Pomp, A.; Gallagher, D. Validity of bioelectrical impedance analysis for measuring changes in body water and percent fat after bariatric surgery. Obes. Surg. 2014, 24, 847–854. [Google Scholar] [CrossRef]
- Ozeki, Y.; Masaki, T.; Yoshida, Y.; Okamoto, M.; Anai, M.; Gotoh, K.; Endo, Y.; Ohta, M.; Inomata, M.; Shibata, H. Bioelectrical impedance analysis results for estimating body composition are associated with glucose metabolism following laparoscopic sleeve gastrectomy in obese Japanese patients. Nutrients 2018, 10, 1456. [Google Scholar] [CrossRef]
- Vassilev, G.; Hasenberg, T.; Krammer, J.; Kienle, P.; Ronellenfitsch, U.; Otto, M. The phase angle of the bioelectrical impedance analysis as predictor of post-bariatric weight loss outcome. Obes. Surg. 2017, 27, 665–669. [Google Scholar] [CrossRef]
- Otto, M.; Elrefai, M.; Krammer, J.; Weiß, C.; Kienle, P.; Hasenberg, T. Sleeve gastrectomy and Roux-en-Y gastric bypass lead to comparable changes in body composition after adjustment for initial body mass index. Obes. Surg. 2016, 26, 479–485. [Google Scholar] [CrossRef]
- Lear, S.A.; Kohli, S.; Bondy, G.P.; Tchernof, A.; Sniderman, A.D. Ethnic variation in fat and lean body mass and the association with insulin resistance. J. Clin. Endocrinol. Metab. 2009, 94, 4696–4702. [Google Scholar] [CrossRef]
- Kodama, K.; Tojjar, D.; Yamada, S.; Toda, K.; Patel, C.J.; Butte, A.J. Ethnic differences in the relationship between insulin sensitivity and insulin response: A systematic review and meta-analysis. Diabetes Care 2013, 36, 1789–1796. [Google Scholar] [CrossRef] [PubMed]
- Kadowaki, S.; Miura, K.; Kadowaki, T.; Fujiyoshi, A.; El-Saed, A.; Masaki, K.H.; Okamura, T.; Edmundowicz, D.; Rodriguez, B.L.; Nakamura, Y.; et al. International Comparison of Abdominal Fat Distribution Among Four Populations: The ERA-JUMP Study. Metab. Syndr. Relat. Disord. 2018, 16, 166–173. [Google Scholar] [CrossRef] [PubMed]
- Gujral, U.P.; Weber, M.B.; Staimez, L.R.; Narayan, K.M.V. Diabetes Among Non-Overweight Individuals: An Emerging Public Health Challenge. Curr. Diab Rep. 2018, 18, 60. [Google Scholar] [CrossRef] [PubMed]
- Ohta, M.; Kai, S.; Iwashita, Y.; Endo, Y.; Hirashita, Y.; Eguchi, H.; Kitano, S. Initial experience in laparoscopic sleeve gastrectomy for Japanese morbid obesity. Asian J. Endosc. Surg. 2009, 2, 68–72. [Google Scholar] [CrossRef]
- Endo, Y.; Ohta, M.; Kawamura, M.; Fujinaga, A.; Nakanuma, H.; Watanabe, K.; Kawasaki, T.; Masuda, T.; Hirashita, T.; Inomata, M. Gastric wall thickness and linear staple height in sleeve gastrectomy in Japanese patients with obesity. Obes. Surg. 2022, 32, 349–354. [Google Scholar] [CrossRef]
- Brethauer, S.A.; El Kim, J.; Chaar, M.; Papasavas, P.; Eisenberg, D.; Rogers, A.; Ballem, N.; Kligman, M.; Kothari, S.; ASMBS Clinical Issues Committee. Standardized outcomes reporting in metabolic and bariatric surgery. Surg. Obes. Relat. Dis. 2015, 11, 489–506. [Google Scholar] [CrossRef]
- Grover, B.T.; Morell, M.C.; Kothari, S.N.; Borgert, A.J.; Kallies, K.J.; Baker, M.T. Defining weight loss after bariatric surgery: A call for standardization. Obes. Surg. 2019, 29, 3493–3499. [Google Scholar] [CrossRef]
- van de Laar, A.W.; Van Rijswijk, A.S.; Kakar, H.; Bruin, S.C. Sensitivity and specificity of 50% excess weight loss (50%EWL) and twelve other bariatric criteria for weight loss success. Obes. Surg. 2018, 28, 2297–2304. [Google Scholar] [CrossRef]
- Ozeki, Y.; Masaki, T.; Yoshida, Y.; Okamoto, M.; Anai, M.; Gotoh, K.; Endo, Y.; Ohta, M.; Inomata, M.; Shibata, H. Relationships between computed tomography-assessed density, abdominal fat volume, and glucose metabolism after sleeve gastrectomy in Japanese patients with obesity. Endocr. J. 2019, 66, 605–613. [Google Scholar] [CrossRef]
- Genders, A.J.; Holloway, G.P.; Bishop, D.J. Are alterations in skeletal muscle mitochondria a cause or consequence of insulin resistance? Int. J. Mol. Sci. 2020, 21, 6948. [Google Scholar] [CrossRef]
- Schauer, P.R.; Bhatt, D.L.; Kirwan, J.P.; Wolski, K.; Brethauer, S.A.; Navaneethan, S.D.; Aminian, A.; Pothier, C.E.; Kim, E.S.; Nissen, S.E.; et al. Bariatric surgery versus intensive medical therapy for diabetes—3-year outcomes. N. Engl. J. Med. 2014, 370, 2002–2013. [Google Scholar] [CrossRef] [PubMed]
- Carlsson, L.M.S.; Sjöholm, K.; Jacobson, P.; Andersson-Assarsson, J.C.; Svensson, P.A.; Taube, M.; Carlsson, B.; Peltonen, M. Life expectancy after bariatric surgery in the Swedish obese subjects study. N. Engl. J. Med. 2020, 383, 1535–1543. [Google Scholar] [CrossRef] [PubMed]
- Mingrone, G.; Panunzi, S.; De Gaetano, A.; Guidone, C.; Iaconelli, A.; Capristo, E.; Chamseddine, G.; Bornstein, S.R.; Rubino, F. Metabolic surgery versus conventional medical therapy in patients with type 2 diabetes: 10-year follow-up of an open-label, single-centre, randomised controlled trial. Lancet 2021, 397, 293–304. [Google Scholar] [CrossRef] [PubMed]
- Courcoulas, A.P.; Patti, M.E.; Hu, B.; Arterburn, D.E.; Simonson, D.C.; Gourash, W.F.; Jakicic, J.M.; Vernon, A.H.; Beck, G.J.; Schauer, P.R.; et al. Long-term outcomes of medical management vs bariatric surgery in type 2 diabetes. JAMA 2024, 331, 654–664. [Google Scholar] [CrossRef]
- Baad, V.M.A.; Bezerra, L.R.; de Holanda, N.C.P.; Dos Santos, A.C.O.; da Silva, A.A.M.; Bandeira, F.; Cavalcante, T.C.F. Body Composition, Sarcopenia and Physical Performance After Bariatric Surgery: Differences Between Sleeve Gastrectomy and Roux-En-Y Gastric Bypass. Obes. Surg. 2022, 32, 3830–3838. [Google Scholar] [CrossRef]
Pre-LSG | 6 Months | 1 Year | 2 Years | 3 Years | |
---|---|---|---|---|---|
Body weight (kg) | 116.1 ± 24.4 | 82.4 ± 17.2 ** | 80.0 ± 18.5 ** | 81.6 ± 22.0 ** | 84.6 ± 21.6 ** |
%TBWL | 28.5 ± 8.3 | 30.7 ± 10.5 | 29.6 ± 12.7 | 27.2 ± 11.9 | |
%EBWL | 60.6 ± 19.5 | 64.8 ± 23.5 | 63.0 ± 27.7 | 57.3 ± 24.7 | |
BMI (kg/m2) | 43.7 ± 8.7 | 31.4 ± 6.7 ** | 30.2 ± 6.5 ** | 30.4 ± 7.4 ** | 31.7 ± 7.6 ** |
Systolic blood pressure (mmHg) | 137.0 ± 17.5 | 119.9 ± 19.4 ** | 120.8 ± 16.0 ** | 125.1 ± 18.0 ** | 125.3 ± 16.6 ** |
Diastolic blood pressure (mmHg) | 83.7 ± 12.4 | 73.0 ± 11.4 ** | 72.7 ± 11.1 ** | 75.6 ± 12.5 ** | 75.5 ± 12.5 ** |
Fasting plasma glucose (mg/dL) | 116.5 ± 35.2 | 99.8 ± 26.7 ** | 96.8 ± 20.3 ** | 97.5 ± 26.9 ** | 92.9 ± 24.6 ** |
HbA1c (%) | 6.8 ± 1.3 | 5.6 ± 0.8 ** | 5.7 ± 0.9 ** | 5.7 ± 0.9 ** | 5.7 ± 0.8 ** |
Triglycerides (mg/dL) | 170.3 ± 84.8 | 103.4 ± 47.5 ** | 100.3 ± 77.8 ** | 97.4 ± 49.2 ** | 100.1 ± 55.2 ** |
HDL cholesterol (mg/dL) | 48.1 ± 11.1 | 58.5 ± 16.2 ** | 63.7 ± 16.3 ** | 68.0 ± 19.0 ** | 70.6 ± 19.5 ** |
LDL cholestrol (mg/dL) | 125.4 ± 32.3 | 121.5 ± 30.7 | 119.2 ± 32.1 | 112.6 ± 29.4 | 111.4 ± 29.0 |
BUN (mg/dL) | 12.6 ± 3.8 | 13.2 ± 4.7 | 14.1 ± 4.3 | 13.6 ± 4.7 | 13.7 ± 4.1 |
Creatinine (mg/dL) | 0.7 ± 0.2 | 0.7 ± 0.1 * | 0.7 ± 0.2 | 0.7 ± 0.2 ** | 0.7 ± 0.2 ** |
AST (IU/L) | 35.0 ± 26.1 | 17.1 ± 5.5 ** | 17.7 ± 4.5 ** | 17.7 ± 5.3 ** | 18.2 ± 4.5 ** |
ALT (IU/L) | 49.6 ± 37.6 | 14.6 ± 5.8 ** | 16.5 ± 6.9 ** | 16.0 ± 7.5 ** | 17.5 ± 8.4 ** |
GTP (IU/L) | 48.3 ± 30.5 | 17.9 ± 12.0 ** | 16.6 ± 7.4 ** | 16.3 ± 7.5 ** | 17.9 ± 8.2 ** |
Antidiabetic drugs use (%, n) | 50.0(24/48) | 6.2(3/48) | 6.2(3/48) | 12.5(6/48) | 14.6(7/48) |
Antihypertensive drugs use (%, n) | 66.7(32/48) | 14.6(7/48) | 25.0(12/48) | 27.1(13/48) | 22.9(11/48) |
Lipid-lowering drugs use (%, n) | 29.2(14/48) | 16.7(8/48) | 16.7(8/48) | 25.0(12/48) | 27.1(13/48) |
Pre-LSG | 6 Months | 1 Year | 2 Years | 3 Years | |
---|---|---|---|---|---|
FM (kg) | 53.2 ± 15.1 | 30.0 ± 13.1 * | 27.8 ± 13.0 * | 29.2 ± 15.5 * | 32.1 ± 15.6 * |
FM (%) | 47.3 ± 6.5 | 35.7 ± 10.0 * | 33.9 ± 9.4 * | 34.6 ± 10.5 * | 37.2 ± 10.0 * |
Total MM (kg) | 55.2 ± 10.2 | 48.9 ± 9.4 * | 48.6 ± 9.3 * | 48.4 ± 9.8 * | 48.1 ± 9.6 * |
Total MM/BW | 0.50 ± 0.06 | 0.60 ± 0.09 * | 0.62 ± 0.09 * | 0.61 ± 0.10 * | 0.59 ± 0.09 * |
Skeletal MM (kg) | 32.4 ± 6.4 | 28.3 ± 5.9 * | 28.1 ± 5.9 * | 28.0 ± 6.2 * | 27.9 ± 6.1 * |
Skeletal MM/BW | 0.29 ± 0.04 | 0.35 ± 0.06 * | 0.36 ± 0.05 * | 0.36 ± 0.06 * | 0.35 ± 0.07 * |
Upper Skeletal MM/BW | 0.06 ± 0.01 | 0.07 ± 0.01 * | 0.07 ± 0.01 * | 0.07 ± 0.01 * | 0.07 ± 0.01 * |
Lower Skeletal MM/BW | 0.16 ± 0.03 | 0.20 ± 0.03 * | 0.20 ± 0.03 * | 0.20 ± 0.03 * | 0.20 ± 0.04 * |
Body fluid | 42.0 ± 9.6 | 37.2 ± 8.5 * | 37.0 ± 8.5 * | 36.8 ± 8.8 * | 36.6 ± 8.7 * |
Bone mineral content | 2.95 ± 0.72 | 2.98 ± 0.57 | 2.96 ± 0.54 | 2.91 ± 0.54 * | 2.86 ± 0.53 * |
The ratio of extra cellular fluid | 0.387 ± 0.009 | 0.394 ± 0.009 * | 0.394 ± 0.010 * | 0.393 ± 0.009 * | 0.391 ± 0.008 * |
Variables | t-Value | p-Value |
---|---|---|
FM | 5.44 | <0.01 * |
% FM | −0.40 | 0.69 |
Total MM | 1.01 | 0.31 |
%Total MM | −0.29 | 0.77 |
Upper Skeletal MM/BW | 0.91 | 0.37 |
Lower Skeletal MM/BW | −0.59 | 0.56 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ozeki, Y.; Masaki, T.; Miyamoto, S.; Yoshida, Y.; Okamoto, M.; Gotoh, K.; Endo, Y.; Inomata, M.; Shibata, H. Positive Changes in Body Composition and Profiles of Individuals with Diabetes 3 Years Following Laparoscopic Sleeve Gastrectomy in Japanese Patients with Obesity. Nutrients 2024, 16, 3926. https://doi.org/10.3390/nu16223926
Ozeki Y, Masaki T, Miyamoto S, Yoshida Y, Okamoto M, Gotoh K, Endo Y, Inomata M, Shibata H. Positive Changes in Body Composition and Profiles of Individuals with Diabetes 3 Years Following Laparoscopic Sleeve Gastrectomy in Japanese Patients with Obesity. Nutrients. 2024; 16(22):3926. https://doi.org/10.3390/nu16223926
Chicago/Turabian StyleOzeki, Yoshinori, Takayuki Masaki, Shotaro Miyamoto, Yuichi Yoshida, Mitsuhiro Okamoto, Koro Gotoh, Yuichi Endo, Masafumi Inomata, and Hirotaka Shibata. 2024. "Positive Changes in Body Composition and Profiles of Individuals with Diabetes 3 Years Following Laparoscopic Sleeve Gastrectomy in Japanese Patients with Obesity" Nutrients 16, no. 22: 3926. https://doi.org/10.3390/nu16223926
APA StyleOzeki, Y., Masaki, T., Miyamoto, S., Yoshida, Y., Okamoto, M., Gotoh, K., Endo, Y., Inomata, M., & Shibata, H. (2024). Positive Changes in Body Composition and Profiles of Individuals with Diabetes 3 Years Following Laparoscopic Sleeve Gastrectomy in Japanese Patients with Obesity. Nutrients, 16(22), 3926. https://doi.org/10.3390/nu16223926