Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Bariatric Surgery

Trends in insulin-like growth factor-1 levels after bariatric surgery: a systematic review and meta-analysis

International Journal of Obesity volume 46, pages 891–900 (2022)Cite this article

Subjects

A Correction to this article was published on 08 February 2022

This article has been updated

Abstract

According to studies, there are many inconsistencies in how IGF-1 levels change after bariatric surgery compared to before surgery, as well as its effects. These discrepancies can be attributed to various factors such as age, body mass index (BMI), and duration of intervention. Therefore, the aim of this study was to evaluate the level of insulin-like growth factor-1 (IGF-1) after bariatric surgery. A systematic review and meta-analysis based on the PRISMA guidelines was conducted from inception until 2021. From 1871 articles initially selected, 24 studies with 28 treatment arms met the eligible criteria and were included. Pooled findings from the random-effects model indicated that IGF-1 levels increased significantly [weighted mean difference (WMD) = 8.84 ng/ml; 95% confidence interval (CI) 0.30–17.39; p = 0.043] after bariatric surgery compared to before surgery. No significant heterogeneity was noted among the studies (Cochran Q test, p = 0.90, I2 = 0.0%). In subgroup analysis, bariatric surgery significantly increased IGF-1 levels at age <40 years but not at age ≤40 years. Bariatric surgery is capable of increasing the IGF-1 levels compared to the period prior to surgery but with a modest clinical magnitude.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Data are available on request due to privacy/ethical restrictions.

Change history

References

  1. Blüher M. Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol. 2019;15:288–98.

    Article  PubMed  Google Scholar 

  2. Santos HO, Lavie CJ. Weight loss and its influence on high-density lipoprotein cholesterol (HDL-C) concentrations: A noble clinical hesitation. Clin Nutr ESPEN. 2021;42:90–2.

    Article  PubMed  Google Scholar 

  3. Doyle SL, Lysaght J, Reynolds J. Obesity and post‐operative complications in patients undergoing non‐bariatric surgery. Obes Rev. 2010;11:875–86.

    Article  CAS  PubMed  Google Scholar 

  4. Mingrone G, Panunzi S, De Gaetano A, Guidone C, Iaconelli A, Nanni G, et al. Bariatric–metabolic surgery versus conventional medical treatment in obese patients with type 2 diabetes: 5 year follow-up of an open-label, single-centre, randomised controlled trial. Lancet. 2015;386:964–73.

    Article  PubMed  Google Scholar 

  5. Holst JJ, Madsbad S, Bojsen-Møller KN, Svane MS, Jørgensen NB, Dirksen C, et al. Mechanisms in bariatric surgery: gut hormones, diabetes resolution, and weight loss. Surg Obes Relat Dis. 2018;14:708–14.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Dimitriadis GK, Randeva MS, Miras AD. Potential hormone mechanisms of bariatric surgery. Curr Obes Rep. 2017;6:253–65.

    Article  PubMed  PubMed Central  Google Scholar 

  7. AsghariHanjani N, Vafa M. The role of IGF-1 in obesity, cardiovascular disease, and cancer. Med J Islam Repub Iran. 2019;33:56.

    PubMed  PubMed Central  Google Scholar 

  8. Maccario M, Grottoli S, Procopio M, Oleandri SE, Rossetto R, Gauna C, et al. The GH/IGF-I axis in obesity: influence of neuro-endocrine and metabolic factors. Int J Obes Relat Metab Disord. 2000;24:S96–9.

    Article  CAS  PubMed  Google Scholar 

  9. Frystyk J. Free insulin-like growth factors–measurements and relationships to growth hormone secretion and glucose homeostasis. Growth Horm IGF Res. 2004;14:337–75.

    Article  CAS  PubMed  Google Scholar 

  10. Al-Regaiey K, Alshubrami S, Al-Beeshi I, Alnasser T, Alwabel A, Al-Beladi H, et al. Effects of gastric sleeve surgery on the serum levels of GH, IGF-1 and IGF-binding protein 2 in healthy obese patients. BMC Gastroenterol. 2020;20:1–6.

    Article  CAS  Google Scholar 

  11. Brynskov T, Laugesen CS, Floyd AK, Frystyk J, Sørensen TL. The IGF-axis and diabetic retinopathy before and after gastric bypass surgery. Obes Surg. 2017;27:408–15.

    Article  PubMed  Google Scholar 

  12. Itariu BK, Zeyda M, Prager G, Stulnig TM. Insulin-like growth factor 1 predicts post-load hypoglycemia following bariatric surgery: a prospective cohort study. PLoS ONE. 2014;9:e94613.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Hussain MA, Schmitz O, Mengel A, Keller A, Christiansen JS, Zapf J, et al. Insulin-like growth factor I stimulates lipid oxidation, reduces protein oxidation, and enhances insulin sensitivity in humans. J Clin Investig. 1993;92:2249–2256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Pellitero S, Granada ML, Martinez E, Balibrea JM, Guanyabens E, Serra A, et al. IGF1 modifications after bariatric surgery in morbidly obese patients: potential implications of nutritional status according to specific surgical technique. Eur J Endocrinol. 2013;169:695–703.

    Article  CAS  PubMed  Google Scholar 

  15. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. System Rev. 2015;4:1.

    Article  Google Scholar 

  16. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25:603–5.

    Article  PubMed  Google Scholar 

  17. Higgins J. Cochrane handbook for systematic reviews of interventions. Version 5.1. 0 [updated March 2011]. The Cochrane Collaboration; 2011. www.cochrane-handbook.org.

  18. Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol. 2005;5:13.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bruna M, Gumbau V, Guaita M, Canelles E, Mulas C, Basés C, et al. Prospective study of gluco-lipidic hormone and peptide levels in morbidly obese patients after sleeve gastrectomy. Cir Esp. 2014;92:175–81.

    Article  PubMed  Google Scholar 

  22. Gómez JM, Vilarrasa N, Masdevall C, Pujol J, Solano E, Soler J, et al. Regulation of bone mineral density in morbidly obese women: a cross-sectional study in two cohorts before and after bypass surgery. Obes Surg. 2009;19:345–50.

    Article  PubMed  Google Scholar 

  23. Di Somma C, Angrisani L, Rota F, Savanelli MC, Cascella T, Belfiore A, et al. GH and IGF-I deficiency are associated with reduced loss of fat mass after laparoscopic-adjustable silicone gastric banding. Clin Endocrinol. 2008;69:393–9.

    Article  CAS  Google Scholar 

  24. Galli G, Pinchera A, Piaggi P, Fierabracci P, Giannetti M, Querci G, et al. Serum insulin-like growth factor-1 concentrations are reduced in severely obese women and raise after weight loss induced by laparoscopic adjustable gastric banding. Obes Surg. 2012;22:1276–80.

    Article  PubMed  Google Scholar 

  25. Guglielmi V, Bellia A, Gentileschi P, Lombardo M, D’Adamo M, Lauro D, et al. Parathyroid hormone in surgery-induced weight loss: no glucometabolic effects but potential adaptive response to skeletal loading. Endocrine. 2018;59:288–95.

    Article  CAS  PubMed  Google Scholar 

  26. Kim TY, Schwartz AV, Li X, Xu K, Black DM, Petrenko DM, et al. Bone marrow fat changes after gastric bypass surgery are associated with loss of bone mass. J Bone Miner Res. 2017;32:2239–47.

    Article  CAS  PubMed  Google Scholar 

  27. Mora MEV, Manco M, Capristo E, Guidone C, Iaconelli A, Gniuli D, et al. Growth hormone and ghrelin secretion in severely obese women before and after bariatric surgery. Obesity. 2007;15:2012–8.

    Article  CAS  Google Scholar 

  28. Poulos J, Leggett-Frazier N, Khazanie P, Long S, Sportsman R, MacDonald K, et al. Circulating insulin-like growth factor I concentrations in clinically severe obese patients with and without NIDDM in response to weight loss. Hormone Metab Res. 1994;26:478–80.

    Article  CAS  Google Scholar 

  29. Stoeckli R, Chanda R, Langer I, Keller U. Changes of body weight and plasma ghrelin levels after gastric banding and gastric bypass. Obesity Res. 2004;12:346–50.

    Article  CAS  Google Scholar 

  30. Vilarrasa N, Gómez JM, Elio I, Gómez-Vaquero C, Masdevall C, Pujol J, et al. Evaluation of bone disease in morbidly obese women after gastric bypass and risk factors implicated in bone loss. Obes Surg. 2009;19:860–6.

    Article  PubMed  Google Scholar 

  31. Vilarrasa N, San José P, García I, Gómez-Vaquero C, Miras PM, de Gordejuela AGR, et al. Evaluation of bone mineral density loss in morbidly obese women after gastric bypass: 3-year follow-up. Obes Surg. 2011;21:465–72.

    Article  PubMed  Google Scholar 

  32. Wolf P, Winhofer Y, Smajis S, Kruschitz R, Schindler K, Gessl A, et al. Hormone substitution after gastric bypass surgery in patients with hypopituitarism secondary to craniopharyngioma. Endocr Pract. 2016;22:595–601.

    Article  PubMed  Google Scholar 

  33. Juiz-Valiña P, Pena-Bello L, Cordido M, Outeiriño-Blanco E, Pértega S, Varela-Rodriguez B, et al. Altered GH-IGF-1 axis in severe obese subjects is reversed after bariatric surgery-induced weight loss and related with low-grade chronic inflammation. J Clin Med. 2020;9:2614.

    Article  PubMed Central  CAS  Google Scholar 

  34. Katsogiannos P, Kamble PG, Wiklund U, Sundbom M, Espes D, Hammar U, et al. Rapid changes in neuroendocrine regulation may contribute to reversal of type 2 diabetes after gastric bypass surgery. Endocrine. 2020;67:344–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. De Marinis L, Bianchi A, Mancini A, Gentilella R, Perrelli M, Giampietro A, et al. Growth hormone secretion and leptin in morbid obesity before and after biliopancreatic diversion: relationships with insulin and body composition. J Clin Endocrinol Metab. 2004;89:174–80.

    Article  PubMed  CAS  Google Scholar 

  36. De Marinis L, Mancini A, Valle D, Tacchino R, Bianchi A, Gentilella R, et al. Evaluation of pre-and postprandial growth hormone (GH)-releasing hormone-induced GH response in subjects with persistent body weight normalisation after biliopancreatic diversion. Int J Obes. 1998;22:1011–8.

    Article  CAS  Google Scholar 

  37. Engström BE, Burman P, Holdstock C, Ohrvall M, Sundbom M, Karlsson FA. Effects of gastric bypass on the GH/IGF-I axis in severe obesity–and a comparison with GH deficiency. Eur J Endocrinol. 2006;154:53–9.

    Article  CAS  Google Scholar 

  38. Giusti V, Gasteyger C, Suter M, Heraief E, Gaillard R, Burckhardt P. Gastric banding induces negative bone remodelling in the absence of secondary hyperparathyroidism: potential role of serum C telopeptides for follow-up. Int J Obes. 2005;29:1429–35.

    Article  CAS  Google Scholar 

  39. Juiz-Valiña P, Outeiriño-Blanco E, Pértega S, Varela-Rodríguez BM, García-Brao MJ, Mena E, et al. Effect of weight loss after bariatric surgery on thyroid-stimulating hormone levels in euthyroid patients with morbid obesity. Nutrients. 2019;11:1121.

    Article  PubMed Central  CAS  Google Scholar 

  40. Pugnale N, Giusti V, Suter M, Zysset E, Heraief E, Gaillard R, et al. Bone metabolism and risk of secondary hyperparathyroidism 12 months after gastric banding in obese pre-menopausal women. Int J Obes. 2003;27:110–16.

    Article  CAS  Google Scholar 

  41. Elmlinger MW, Kühnel W, Weber MM, Ranke MB. Reference ranges for two automated chemiluminescent assays for serum insulin-like growth factor I (IGF-I) and IGF-binding protein 3 (IGFBP-3). Clin Chem Lab Med. 2004;42:654–64.

    Article  CAS  PubMed  Google Scholar 

  42. Xie M, Zhong Y, Xue Q, Wu M, Deng X, OS H, et al. Impact of dehydroepianrosterone (DHEA) supplementation on serum levels of insulin-like growth factor 1 (IGF-1): A dose-response meta-analysis of randomized controlled trials. Exp Gerontol. 2020;136:110949.

    Article  CAS  PubMed  Google Scholar 

  43. Kreitschmann-Andermahr I, Suarez P, Jennings R, Evers N, Brabant G. GH/IGF-I regulation in obesity–mechanisms and practical consequences in children and adults. Horm Res Paediatr. 2010;73:153–60.

    Article  CAS  PubMed  Google Scholar 

  44. Schneider HJ, Saller B, Klotsche J, März W, Erwa W, Wittchen HU, et al. Opposite associations of age-dependent insulin-like growth factor-I standard deviation scores with nutritional state in normal weight and obese subjects. Eur J Endocrinol. 2006;154:699–706.

    Article  CAS  PubMed  Google Scholar 

  45. Aguirre GA, De Ita JR, de la Garza RG, Castilla-Cortazar I. Insulin-like growth factor-1 deficiency and metabolic syndrome. J Transl Med. 2016;14:3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Edén Engström B, Burman P, Holdstock C, Ohrvall M, Sundbom M, Karlsson FA. Effects of gastric bypass on the GH/IGF-I axis in severe obesity–and a comparison with GH deficiency. Eur J Endocrinol. 2006;154:53–9.

    Article  PubMed  CAS  Google Scholar 

  47. Frystyk J, Vestbo E, Skjaerbaek C, Mogensen CE, Orskov H. Free insulin-like growth factors in human obesity. Metabolism: clinical and experimental. 1995;44:37–44.

    Article  CAS  Google Scholar 

  48. Frystyk J, Brick DJ, Gerweck AV, Utz AL, Miller KK. Bioactive insulin-like growth factor-I in obesity. J Clin Endocrinol Metab. 2009;94:3093–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Laron Z. Insulin-like growth factor 1 (IGF-1): a growth hormone. Mol Pathol. 2001;54:311–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Shadid S, Jensen MD. Effects of growth hormone administration in human obesity. Obes Res. 2003;11:170–5.

    Article  CAS  PubMed  Google Scholar 

  51. Mekala KC, Tritos NA. Effects of recombinant human growth hormone therapy in obesity in adults: a meta analysis. J Clin Endocrinol Metab. 2009;94:130–7.

    Article  CAS  PubMed  Google Scholar 

  52. Savastano S, Di Somma C, Angrisani L, Orio F, Longobardi S, Lombardi G, et al. Growth hormone treatment prevents loss of lean mass after bariatric surgery in morbidly obese patients: results of a pilot, open, prospective, randomized, controlled study. J Clin Endocrinol Metab. 2009;94:817–26.

    Article  CAS  PubMed  Google Scholar 

  53. Lewitt MS. The role of the growth hormone/insulin-like growth factor system in visceral adiposity. Biochem Insights. 2017;10:1178626417703995.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Grimberg A. Mechanisms by which IGF-I may promote cancer. Cancer Biol Ther. 2003;2:630–635.

    Article  CAS  PubMed  Google Scholar 

  55. Teixeira FJ, Santos HO, Howell SL, Pimentel GD. Whey protein in cancer therapy: a narrative review. Pharmacological research. 2019;144:245–56.

    Article  CAS  PubMed  Google Scholar 

  56. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med. 2003;348:1625–38.

    Article  PubMed  Google Scholar 

  57. Pischon T, Nöthlings U, Boeing H. Obesity and cancer. Proc Nutr Soc. 2008;67:128–45.

    Article  PubMed  Google Scholar 

  58. Stone TW, McPherson M, Gail Darlington L. Obesity and cancer: existing and new hypotheses for a causal connection. EBioMedicine. 2018;30:14–28.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Ligibel JA, Alfano CM, Courneya KS, Demark-Wahnefried W, Burger RA, Chlebowski RT, et al. American Society of Clinical Oncology position statement on obesity and cancer. J Clin Oncol. 2014;32:3568–74.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study is related to the project No. 1399/4235 from Student Research Committee, Shahid Beheshti University of Medical Sciences, Tehran, Iran. We also appreciate the “Student Research Committee” and “Research & Technology Chancellor” in Shahid Beheshti University of Medical Sciences for their financial support of this study.

Author information

Author notes

  1. These authors contributed equally: Mohammad Hassan Sohouli, Mansoureh Baniasadi.

Authors and Affiliations

  1. Student Research Committee, Department of Clinical Nutrition and Dietetics, Faculty of Nutrition and Food Technology, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Mohammad Hassan Sohouli

  2. Cancer Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Mohammad Hassan Sohouli & Mansoureh Baniasadi

  3. Pediatric Gastroenterology, Hepatology and Nutrition Research Center, Research Institute for Children’s Health, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Raheleh Nabavizadeh & Somaye Fatahi

  4. Postgraduate Program in Collective Health, Federal University of Maranhão, São Luís, Maranhão, Brazil

    Elma Izze da Silva Magalhães

  5. School of Medicine, Federal University of Uberlandia (UFU), Uberlandia, Minas Gerais, Brazil

    Heitor O. Santos

  6. Student Research Committee, Faculty of Public Health Branch, Iran University of Medical Sciences, Tehran, Iran

    Somaye Fatahi

  7. Department of Pediatric Endocrinology and Metabolism, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

    Mojtaba Lotfi

Authors
  1. Mohammad Hassan Sohouli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mansoureh Baniasadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Raheleh Nabavizadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elma Izze da Silva Magalhães
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Heitor O. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Somaye Fatahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mojtaba Lotfi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ML, MB, RN, and MHS contributed in conception, design, and statistical analysis. MHS, HS, EM, and SF contributed in data collection and manuscript drafting. MHS and ML supervised the study. All authors approved the final version of the manuscript.

Corresponding author

Correspondence to Mojtaba Lotfi.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethical approval and consent to participate

This study was approved by the research council and ethics committee Shahid Beheshti University of Medical Sciences, Tehran, Iran.

Additional information

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

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sohouli, M.H., Baniasadi, M., Nabavizadeh, R. et al. Trends in insulin-like growth factor-1 levels after bariatric surgery: a systematic review and meta-analysis. Int J Obes 46, 891–900 (2022). https://doi.org/10.1038/s41366-021-01051-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41366-021-01051-6

Search

Advanced search

Quick links