Circulating biomarker profile changes in obese patients undergoing bariatric surgery

Authors

  • Natalya Sushentseva Translational Biomedicine Laboratory, City Hospital no. 40, ul. Borisova, 9, Saint Petersburg, 197706, Russian Federation https://orcid.org/0000-0002-5100-5229
  • Svetlana Apalko Translational Biomedicine Laboratory, City Hospital no. 40, ul. Borisova, 9, Saint Petersburg, 197706, Russian Federation https://orcid.org/0000-0002-3853-4185
  • Oleg Popov Translational Biomedicine Laboratory, City Hospital no. 40, ul. Borisova, 9, Saint Petersburg, 197706, Russian Federation; Faculty of Medicine, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0003-1778-0165
  • Irina Polkovnikova Translational Biomedicine Laboratory, City Hospital no. 40, ul. Borisova, 9, Saint Petersburg, 197706, Russian Federation; Faculty of Medicine, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-9178-8512
  • Evgeny Vasiliev Translational Biomedicine Laboratory, City Hospital no. 40, ul. Borisova, 9, Saint Petersburg, 197706, Russian Federation
  • Dmitriy Gladyshev Translational Biomedicine Laboratory, City Hospital no. 40, ul. Borisova, 9, Saint Petersburg, 197706, Russian Federation https://orcid.org/0000-0001-5318-2619
  • Vladimir Salukhov S. M. Kirov Military Medical Academy, ul. Akademika Lebedeva, 6, Saint Petersburg, 194044, Russian Federation https://orcid.org/0000-0003-1851-0941
  • Sergey Scherbak Translational Biomedicine Laboratory, City Hospital no. 40, ul. Borisova, 9, Saint Petersburg, 197706, Russian Federation; Faculty of Medicine, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0001-5036-1259

DOI:

https://doi.org/10.21638/spbu03.2024.103

Abstract

Bariatric surgery (BS) remains the most effective treatment for morbid obesity (MO). It`s relevant to identify biomarkers for predicting the outcome of BS in patients with MO. The aim of the study was to determine the dynamical change in the biomarker levels in patients undergoing BS and apparently healthy donors. Serum and plasma samples were obtained from 66 patients, of which 26 patients with MO (aged 26–72 years) underwent BS, and 40 healthy donors, at the age of 56 ± 10.3 years. Patient samples were obtained the day before BS (first group), 3–7 months after BS (second group), and 7 or more months after BS (third group). Analyte concentrations were determined by multiplex immunoassay on the xMAP platform (Luminex). Spearman’s rank correlation was used. The nature of analyte variability was described by building multiple regression models. In the patients compared with healthy controls, differences in the levels of resistin, PAI1, MCP1, GLP1, leptin, FGF23, adiponectin, adipsin were observed. In patients after BS, the levels of resistin, ANGPTL6, FGF21, and leptin changed. In patients over 55 years old compared with younger patients, differences for total ANGPTL4, amylin, and pancreatic polypeptide were observed. Differences in levels of glucagon, resistin, GLP1 and leptin were noted between men and women. The dynamics of the levels of adipokines and incretins indicates biochemical changes in patients after BS compared with healthy persons.

Keywords:

obesity, biomarkers, bariatric surgery, weight loss, body weight

Downloads

Download data is not yet available.
 

References

Abulmeaty, M. M. A., Ghneim, H. K., Alkhathaami, A., Alnumair, K., Al Zaben, M., Razak, S., and Al-Sheikh, Y. A. 2023. Inflammatory cytokines, redox status, and cardiovascular diseases risk after weight loss via bariatric surgery and lifestyle intervention. Medicina 59(4):751. https://doi.org/10.3390/medicina59040751

Adami, G. F., Scopinaro, N., and Cordera, R. 2016. Adipokine pattern after bariatric surgery: Beyond the weight loss. Obesity Surgery 26(11):2793–2801. https://doi.org/10.1007/s11695-016-2347-1

Arica, P. C., Aydin, S., Zengin, U., Kocael, A., Orhan, A., Zengin, K., Gelisgen, R., Taskin, M., and Uzun, H. 2018. The effects on obesity related peptides of laparoscopic gastric band applications in morbidly obese patients. Journal of Investigative Surgery 31(2):89–95. https://doi.org/10.1080/08941939.2017.1280564

Askarpour, M., Alizadeh, S., Hadi, A., Symonds, M., Miraghajani, M., Sheikhi, A., and Ghaedi, E. 2020. Effect of bariatric surgery on the circulating level of adiponectin, chemerin, plasminogen activator inhibitor-1, leptin, resistin, and visfatin: A systematic review and meta-analysis. Hormone and Metabolic Research 52(04):207–215. https://doi.org/10.1055/a-1129-6785

Bini, S., D’Erasmo, L., Astiarraga, B., Minicocci, I., Palumbo, M., Pecce, V., Polito, L., Di Costanzo, A., Haeusler, R. A., Arca, M., Ferrannini, E., and Camastra, S. 2022. Differential effects of bariatric surgery on plasma levels of ANGPTL3 and ANGPTL4. Nutrition, metabolism, and cardiovascular diseases 32(11):2647–2654. https://doi.org/10.1016/j.numecd.2022.08.019

Bini, S., D’Erasmo, L., Di Costanzo, A., Minicocci, I., Pecce, V., and Arca, M. 2021. The interplay between angiopoietin-like proteins and adipose tissue: Another piece of the relationship between adiposopathy and cardiometabolic diseases? International Journal of Molecular Sciences 22(2):742. https://doi.org/10.3390/ijms22020742

Cinkajzlova, A., Lacinova, Z., Klouckova, J., Kavalkova, P., Trachta, P., Kosak, M., Haluzikova, D., Papezova, H., Mraz, M., and Haluzík, M. 2017. Angiopoietin-like protein 6 in patients with obesity, type 2 diabetes mellitus, and anorexia nervosa: The influence of very low-calorie diet, bariatric surgery, and partial realimentation. Endocrine Research 42(1):22–30. https://doi.org/10.3109/07435800.2016.1169544

Elci, E., Kaya, C., Cim, N., Yildizhan, R., and Elci, G. G. 2017. Evaluation of cardiac risk marker levels in obese and non-obese patients with polycystic ovaries. Gynecological Endocrinology 33(1):43–47. https://doi.org/10.1080/09513590.2016.1203893

Ezzat, S. and Asa, S. L. 2005. FGF receptor signaling at the crossroads of endocrine homeostasis and tumorigenesis. Hormone and Metabolic Research 37(6):355–360. https://doi.org/10.1055/s-2005-870151

Fjeldborg, K., Pedersen, S. B., Møller, H. J., and Richelsen, B. 2017. Reduction in serum fibroblast growth factor-21 after gastric bypass is related to changes in hepatic fat content. Surgery for Obesity and Related Diseases 13(9):1515–1523. https://doi.org/10.1016/j.soard.2017.03.033

Flier, J. S., Cook, K. S., Usher, P., and Spiegelman, B. M. 1987. Severely impaired adipsin expression in genetic and acquired obesity. Science 237(4813):405–408. https://doi.org/10.1126/science.3299706

Formichi, C., Cantara, S., Ciuoli, C., Neri, O., Chiofalo, F., Selmi, F., Tirone, A., Colasanto, G., Di Cosmo, L., Vuolo, G., and Pacini, F. 2014. Weight loss associated with bariatric surgery does not restore short telomere length of severe obese patients after 1 year. Obesity Surgery 24(12):2089–2093. https://doi.org/10.1007/s11695-014-1300-4

Fu, L., John, L. M., Adams, S. H., Yu, X. X., Tomlinson, E., Renz, M., Williams, P. M., Soriano, R., Corpuz, R., Moffat, B., Vandlen, R., Simmons, L., Foster, J., Stephan, J.-P., Tsai, S. P., and Stewart, T. A. 2004. Fibroblast growth factor 19 increases metabolic rate and reverses dietary and leptin-deficient diabetes. Endocrinology 145(6):2594–2603. https://doi.org/10.1210/en.2003-1671

Furbetta, N., Cervelli, R., and Furbetta, F. 2020. Laparoscopic adjustable gastric banding, the past, the present and the future. Annals of Translational Medicine 8(Suppl 1):S4. https://doi.org/10.21037/atm.2019.09.17

Furbetta, N., Gragnani, F., Flauti, G., Guidi, F., and Furbetta, F. 2019. Laparoscopic adjustable gastric banding on 3566 patients up to 20-year follow-up: Long-term results of a standardized technique. Surgery for Obesity and Related Diseases 15(3):409–416. https://doi.org/10.1016/j.soard.2018.12.012

Gagner, M. 2019. For whom the bell tolls? It is time to retire the classic BPD (bilio-pancreatic diversion) operation. Surgery for Obesity and Related Diseases 15(6):1029–1031. https://doi.org/10.1016/j.soard.2019.03.029

Gazioglu, S. B., Akan, G., Atalar, F., and Erten, G. 2015. PAI-1 and TNF-α profiles of adipose tissue in obese cardiovascular disease patients. International Journal of Clinical and Experimental Pathology 8(12):15919–15925.

Hohensinner, P. J., Kaun, C., Ebenbauer, B., Hackl, M., Demyanets, S., Richter, D., Prager, M., Wojta, J., and Rega-Kaun, G. 2018. Reduction of premature aging markers after gastric bypass surgery in morbidly obese patients. Obesity Surgery 28(9):2804–2810. https://doi.org/10.1007/s11695-018-3247-3

Jain, A. K., le Roux, C. W., Puri, P., Tavakkoli, A., Gletsu-Miller, N., Laferrère, B., Kellermayer, R., DiBaise, J. K., Martindale, R. G., and Wolfe, B. M. 2018. Proceedings of the 2017 ASPEN research workshop-gastric bypass: Role of the gut. Journal of Parenteral and Enteral Nutrition 42(2):279–295. https://doi.org/10.1002/jpen.1121

Jakobsen, G. S., Småstuen, M. C., Sandbu, R., Nordstrand, N., Hofsø, D., Lindberg, M., Hertel, J. K., and Hjelmesæth, J. 2018. Association of bariatric surgery vs medical obesity treatment with long-term medical complications and obesity-related comorbidities. JAMA 319(3):291–301. https://doi.org/10.1001/jama.2017.21055

Jiang, Z., Zou, Y., Huang, H., Zheng, F., Dai, X., and Li, Y. 2010. Mechanism of laparoscopic adjustable gastric banding in the treatment of obesity with type 2 diabetes mellitus. Chinese Journal of Gastrointestinal Surgery 13(7):520–523.

Kelly, A. S., Ryder, J. R., Marlatt, K. L., Rudser, K. D., Jenkins, T., and Inge, T. H. 2016. Changes in inflammation, oxidative stress and adipokines following bariatric surgery among adolescents with severe obesity. International Journal of Obesity 40(2):275–280. https://doi.org/10.1038/ijo.2015.174

Kersten, S., Mandard, S., Tan, N. S., Escher, P., Metzger, D., Chambon, P., Gonzalez, F. J., Desvergne, B., and Wahli, W. 2000. Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. The Journal of Biological Chemistry 275(37):28488–28493. https://doi.org/10.1074/jbc.M004029200

Kim, S. H., Chun, H. J., Choi, H. S., Kim, E. S., Keum, B., and Jeen, Y. T. 2016. Current status of intragastric balloon for obesity treatment. World Journal of Gastroenterology 22(24):5495–5504. https://doi.org/10.3748/wjg.v22.i24.5495

Ko, D. S. C. and Delmonico, F. L. 2008. Chapter 7 — Medical Evaluation of the Living Donor; pp. 99–110 in P. J. Morris and S. J. Knechtle (eds), Kidney Transplantation. 6th ed. W. B. Saunders, Philadelphia.

Kuipers, F. and Groen, A. K. 2014. FXR: the key to benefits in bariatric surgery? Nature Medicine 20(4):337–338. https://doi.org/10.1038/nm.3525

Kvalem, I. L., Bergh, I., von Soest, T., Rosenvinge, J. H., Johnsen, T. A., Martinsen, E. W., Mala, T., and Kristinsson, J. A. 2015. A comparison of behavioral and psychological characteristics of patients opting for surgical and conservative treatment for morbid obesity. BMC Obesity 3:6. https://doi.org/10.1186/s40608-016-0084-6

Lejawa, M., Osadnik, K., Czuba, Z., Osadnik, T., and Pawlas, N. 2021. Association of metabolically healthy and unhealthy obesity phenotype with markers related to obesity, diabetes among young, healthy adult men. Analysis of MAGNETIC study. Life 11(12):1350. https://doi.org/10.3390/life11121350

Li, T. and Chiang, J. Y. L. 2014. Bile acid signaling in metabolic disease and drug therapy. Pharmacological Reviews 66(4):948–983. https://doi.org/10.1124/pr.113.008201

Mathus-Vliegen, E. M. H. and de Groot, G. H. 2013. Fasting and meal-induced CCK and PP secretion following intragastric balloon treatment for obesity. Obesity Surgery 23(5):622–633. https://doi.org/10.1007/s11695-012-0834-6

Mathus-Vliegen, E. M. H. and Eichenberger, R. I. 2014. Fasting and meal-suppressed ghrelin levels before and after intragastric balloons and balloon-induced weight loss. Obesity Surgery 24(1):85–94. https://doi.org/10.1007/s11695-013-1053-5

Milek, M., Moulla, Y., Kern, M., Stroh, C., Dietrich, A., Schön, M. R., Gärtner, D., Lohmann, T., Dressler, M., Kovacs, P., Stumvoll, M., Blüher, M., and Guiu-Jurado, E. 2022. Adipsin serum concentrations and adipose tissue expression in people with obesity and type 2 diabetes. International Journal of Molecular Sciences 23(4):2222. https://doi.org/10.3390/ijms23042222

Neuschwander-Tetri, B. A., Loomba, R., Sanyal, A. J., Lavine, J. E., Van Natta, M. L., Abdelmalek, M. F., Chalasani, N., Dasarathy, S., Diehl, A. M., Hameed, B., Kowdley, K. V., McCullough, A., Terrault, N., Clark, J. M., Tonascia, J., Brunt, E. M., Kleiner, D. E., and Doo, E. 2015. Farnesoid X nuclear receptor ligand obeticholic acid for non-cirrhotic, non-alcoholic steatohepatitis (FLINT): A multicentre, randomised, placebo-controlled trial. Lancet 385(9972):956–965. https://doi.org/10.1016/S0140-6736(14)61933-4

Nielsen, M. S., Ritz, C., Chenchar, A., Bredie, W. L. P., Gillum, M. P., and Sjödin, A. 2021. Does FGF21 mediate the potential decrease in sweet food intake and preference following bariatric surgery? Nutrients 13(11):3840. https://doi.org/10.3390/nu13113840

O’Rourke, R. W., Johnson, G. S., Purnell, J. Q., Courcoulas, A. P., Dakin, G. F., Garcia, L., Hinojosa, M., Mitchell, J. E., Pomp, A., Pories, W. J., Spaniolas, K., Flum, D. R., Wahed, A. S., and Wolfe, B. M. 2019. Serum biomarkers of inflammation and adiposity in the LABS cohort: Associations with metabolic disease and surgical outcomes. International Journal of Obesity 43(2):285–296. https://doi.org/10.1038/s41366-018-0088-z

Papadia, F., Carlini, F., Longo, G., Rubartelli, A., Battistini, M., Drago, B., Adami, G. F., Marinari, G., and Camerini, G. 2023. Pyrrhic victory? Long term results of biliopancreatic diversion on type 2 diabetic patients with severe obesity. Surgery for Obesity and Related Diseases 19(10):1110–1117. https://doi.org/10.1016/j.soard.2023.04.300

Patti, M.-E., Houten, S. M., Bianco, A. C., Bernier, R., Larsen, P. R., Holst, J. J., Badman, M. K., Maratos-Flier, E., Mun, E. C., Pihlajamaki, J., Auwerx, J., and Goldfine, A. B. 2009. Serum bile acids are higher in humans with prior gastric bypass: Potential contribution to improved glucose and lipid metabolism. Obesity 17(9):1671–1677. https://doi.org/10.1038/oby.2009.102

Sachan, A., Singh, A., Shukla, S., Aggarwal, S., Mir, I., and Yadav, R. 2020. Serum adipocytokines levels and their association with insulin sensitivity in morbidly obese individuals undergoing bariatric surgery. Journal of Obesity & Metabolic Syndrome 29(4):303–312. https://doi.org/10.7570/jomes20090

Sams, V. G., Blackledge, C., Wijayatunga, N., Barlow, P., Mancini, M., Mancini, G., and Moustaid-Moussa, N. 2016. Effect of bariatric surgery on systemic and adipose tissue inflammation. Surgical Endoscopy 30(8):3499–3504. https://doi.org/10.1007/s00464-015-4638-3

Sjöström, L. 2013. Review of the key results from the Swedish Obese Subjects (SOS) trial — a prospective controlled intervention study of bariatric surgery. Journal of Internal Medicine 273(3):219–234. https://doi.org/10.1111/joim.12012

Thomsen, S. B., Rathcke, C. N., Jørgensen, N. B., Madsbad, S., and Vestergaard, H. 2013. Effects of Roux-en-Y gastric bypass on fasting and postprandial levels of the inflammatory markers YKL-40 and MCP-1 in patients with type 2 diabetes and glucose tolerant subjects. Journal of Obesity 2013:1–10. https://doi.org/10.1155/2013/361781

Vasilenko, M. A., Kirienkova, E. V., Skuratovskaia, D. A., Zatolokin, P. A., Mironyuk, N. I., and Litvinova, L. S. 2017. The role of production of adipsin and leptin in the development of insulin resistance in patients with abdominal obesity. Doklady Biochemistry and Biophysics 475(1):271–276. https://doi.org/10.1134/S160767291704010X

Venables, W. V. and Ripley, B. D. 2013. Modern Applied Statistics with S-PLUS. Springer Science & Business Media.

Viana, E. C., Araujo-Dasilio, K. L., Miguel, G. P. S., Bressan, J., Lemos, E. M., Moyses, M. R., Abreu, G. R. de, Azevedo, J. L. M. C. de, Carvalho, P. S., Passos-Bueno, M. R. S., Errera, F. I. V., and Bissoli, N. S. 2013. Gastric bypass and sleeve gastrectomy: The same impact on IL-6 and TNF-α. Prospective clinical trial. Obesity Surgery 23(8):1252–1261. https://doi.org/10.1007/s11695-013-0894-2

Woelnerhanssen, B., Peterli, R., Steinert, R. E., Peters, T., Borbély, Y., and Beglinger, C. 2011. 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 7(5):561–568. https://doi.org/10.1016/j.soard.2011.01.044

Yen, H.-H., Hsieh, S.-T., Chen, C.-L., Yang, W.-S., Lee, P.-C., Lin, M.-T., Chen, C.-N., and Yang, P.-J. 2020. Circulating diabetic candidate neurotrophic factors, brain-derived neurotrophic factor and fibroblast growth factor 21, in sleeve gastrectomy. Scientific Reports 10(1):5341. https://doi.org/10.1038/s41598-020-62395-z

Biological Communications

Downloads

Published

2024-05-31

How to Cite

Sushentseva, N., Apalko, S., Popov, O., Polkovnikova, I., Vasiliev, E., Gladyshev, D., … Scherbak, S. (2024). Circulating biomarker profile changes in obese patients undergoing bariatric surgery. Biological Communications, 69(1), 26–36. https://doi.org/10.21638/spbu03.2024.103

Issue

Vol. 69 No. 1 (2024)

Section

Full communications

Categories

License

Articles of Biological Communications are open access distributed under the terms of the License Agreement with Saint Petersburg State University, which permits to the authors unrestricted distribution and self-archiving free of charge.