Bariatric Surgery

Effects of bariatric surgery on retinal microvascular architecture in obese patients

Abstract

Study aim

Retinal microvasculature changes reflect systemic small vessel damage from obesity. The impact of bariatric surgery induced weight loss on the microvasculature is relatively unknown. We hypothesized that weight loss following bariatric surgery would be associated with improved structural changes in the retinal microvasculature, reflecting an overall improvement in microvascular health.

Methods

The study included 22 obese subjects scheduled for bariatric surgery (laparoscopic Roux-en-Y gastric bypass or a sleeve gastrectomy) and 15 lean, age-matched controls. Ophthalmic examination, including fundus photography, was performed at baseline and 6-months. Retinal microvasculature caliber was analysed quantitatively using a semi-automated computer program and summarized as central retinal artery equivalent (CRAE) and venular equivalent (CRVE).

Results

Mean weight loss at 6 months was 26.1 kg ± 8 kg in the bariatric surgery group. Retinal artery caliber increased (136.0 ± 1.4 to 141.4 ± 1.4 µm, p = 0.013) and venular caliber decreased (202.9 ± 1.9 to 197.3 ± 1.9 µm, p = 0.046) in the bariatric surgery group by 6 months, with no change in arteriolar (136.6 ± 1.1 to 134.5 ± 1.2, p = 0.222) or venular (195.1 ± 2.1 to 193.3 ± 2.2, p = 0.550) caliber in the control group. The arteriolar to venular ratio increased in the bariatric surgery group, with no change in the control group at 6 months.

Conclusions

The findings suggest obesity-related microvascular changes are reversible after bariatric surgery-induced weight loss. The capacity for the retinal microvasculature to improve following bariatric surgery suggests plasticity of the human microvasculature early in the disease course.

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References

  1. 1.

    Sjostrom L, Peltonen M, Jacobson P, Sjostrom CD, Karason K, Wedel H, et al. Bariatric surgery and long-term cardiovascular events. JAMA. 2012;307:56–65.

  2. 2.

    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.

  3. 3.

    Arterburn D, Bogart A, Coleman KJ, Haneuse S, Selby JV, Sherwood NE, et al. Comparative effectiveness of bariatric surgery vs. nonsurgical treatment of type 2 diabetes among severely obese adults. Obes Res Clin Pract. 2013;7:e258–68.

  4. 4.

    Schauer PR, Mingrone G, Ikramuddin S, Wolfe B. Clinical Outcomes of Metabolic Surgery: Efficacy of Glycemic Control, Weight Loss, and Remission of Diabetes. Diabetes Care. 2016;39:902–11.

  5. 5.

    Lammert A, Hasenberg T, Kraupner C, Schnulle P, Hammes HP. Improved arteriole-to-venule ratio of retinal vessels resulting from bariatric surgery. Obesity. 2012;20:2262–7.

  6. 6.

    Antonio PR, Marta PS, Luis DD, Antonio DP, Manuel ST, Rafael MS, et al. Factors associated with changes in retinal microcirculation after antihypertensive treatment. J Hum Hypertens. 2014;28:310–5.

  7. 7.

    Ting DSW, Tan GSW, Agrawal R, Yanagi Y, Sie NM, Wong CW, et al. Optical Coherence Tomographic Angiography in Type 2 Diabetes and Diabetic Retinopathy. JAMA Ophthalmol. 2017;135:306–12.

  8. 8.

    Murthy VL, Naya M, Foster CR, Gaber M, Hainer J, Klein J, et al. Association between coronary vascular dysfunction and cardiac mortality in patients with and without diabetes mellitus. Circulation. 2012;126:1858–68.

  9. 9.

    Tapp RJ, Ness A, Williams C, Howe LD, Tilling K, Witt N, et al. Mc GTSA and Hughes AD. Differential effects of adiposity and childhood growth trajectories on retinal microvascular architecture. Microcirculation. 2013;20:609–16.

  10. 10.

    Wang JJ, Taylor B, Wong TY, Chua B, Rochtchina E, Klein R, et al. Retinal vessel diameters and obesity: a population-based study in older persons. Obesity. 2006;14:206–14.

  11. 11.

    Boillot A, Zoungas S, Mitchell P, Klein R, Klein B, Ikram MK, et al. Obesity and the microvasculature: a systematic review and meta-analysis. PLoS ONE. 2013;8:e52708.

  12. 12.

    Tapp RJ, Hussain SM, Battista J, Hutri-Kahonen N, Lehtimaki T, Hughes AD, et al. Impact of blood pressure on retinal microvasculature architecture across the lifespan: the Young Finns Study. Microcirculation. 2015;22:146–55.

  13. 13.

    Wang JJ, Mitchell P, Leung H, Rochtchina E, Wong TY, Klein R. Hypertensive retinal vessel wall signs in a general older population: the Blue Mountains Eye Study. Hypertension. 2003;42:534–41.

  14. 14.

    Cheung CY, Ikram MK, Klein R, Wong TY. The clinical implications of recent studies on the structure and function of the retinal microvasculature in diabetes. Diabetologia. 2015;58:871–85.

  15. 15.

    Sabanayagam C, Lye WK, Klein R, Klein BE, Cotch MF, Wang JJ, et al. Retinal microvascular calibre and risk of diabetes mellitus: a systematic review and participant-level meta-analysis. Diabetologia. 2015;58:2476–85.

  16. 16.

    Sabanayagam C, Shankar A, Koh D, Chia KS, Saw SM, Lim SC, et al. Retinal microvascular caliber and chronic kidney disease in an Asian population. Am J Epidemiol. 2009;169:625–32.

  17. 17.

    Wong TY, Klein R, Klein BE, Meuer SM, Hubbard LD. Retinal vessel diameters and their associations with age and blood pressure. Invest Ophthalmol Vis Sci. 2003;44:4644–50.

  18. 18.

    Ding J, Wai KL, McGeechan K, Ikram MK, Kawasaki R, Xie J, et al. and Meta-Eye Study G. Retinal vascular caliber and the development of hypertension: a meta-analysis of individual participant data. J Hypertens. 2014;32:207–15.

  19. 19.

    Wong TY, Islam FM, Klein R, Klein BE, Cotch MF, Castro C, et al. Retinal vascular caliber, cardiovascular risk factors, and inflammation: the multi-ethnic study of atherosclerosis (MESA). Invest Ophthalmol Vis Sci. 2006;47:2341–50.

  20. 20.

    Bruyndonckx L, Hoymans VY, Lemmens K, Ramet J, Vrints CJ. Childhood obesity-related endothelial dysfunction: an update on pathophysiological mechanisms and diagnostic advancements. Pediatr Res. 2016;79:831–7.

  21. 21.

    Gishti O, Jaddoe VW, Hofman A, Wong TY, Ikram MK, Gaillard R. Body fat distribution, metabolic and inflammatory markers and retinal microvasculature in school-age children. The Generation R Study. Int J Obes. 2015;39:1482–7.

  22. 22.

    Sorensen BM, Houben AJ, Berendschot TT, Schouten JS, Kroon AA, van der Kallen CJ, et al. Type 2 diabetes are associated with generalized microvascular dysfunction: the Maastricht Study. Circulation. 2016. Nov 1;134(18):1339–1352

  23. 23.

    Nguyen TT, Wang JJ, Islam FM, Mitchell P, Tapp RJ, Zimmet PZ, et al. Retinal arteriolar narrowing predicts incidence of diabetes: the Australian Diabetes, Obesity and Lifestyle (AusDiab) Study. Diabetes. 2008;57:536–9.

  24. 24.

    Cheung CY, Lamoureux E, Ikram MK, Sasongko MB, Ding J, Zheng Y, et al. Retinal vascular geometry in Asian persons with diabetes and retinopathy. J Diabetes Sci Technol. 2012;6:595–605.

  25. 25.

    Wang L, Wong TY, Sharrett AR, Klein R, Folsom AR, Jerosch-Herold M. Relationship between retinal arteriolar narrowing and myocardial perfusion: multi-ethnic study of atherosclerosis. Hypertension. 2008;51:119–26.

  26. 26.

    Honka H, Koffert J, Hannukainen JC, Tuulari JJ, Karlsson HK, Immonen H, et al. The effects of bariatric surgery on pancreatic lipid metabolism and blood flow. J Clin Endocrinol Metab. 2015;100:2015–23.

  27. 27.

    Helmio M, Victorzon M, Ovaska J, Leivonen M, Juuti A, Jaser N, et al. SLEEVEPASS: a randomized prospective multicenter study comparing laparoscopic sleeve gastrectomy and gastric bypass in the treatment of morbid obesity: preliminary results. Surg Endosc. 2012;26:2521–6.

  28. 28.

    Cheung CY, Tay WT, Mitchell P, Wang JJ, Hsu W, Lee ML, et al. Quantitative and qualitative retinal microvascular characteristics and blood pressure. J Hypertens. 2011;29:1380–91.

  29. 29.

    Cheung CY, Hsu W, Lee ML, Wang JJ, Mitchell P, Lau QP, et al. A new method to measure peripheral retinal vascular caliber over an extended area. Microcirculation. 2010;17:495–503.

  30. 30.

    Liew G, Wang JJ, Cheung N, Zhang YP, Hsu W, Lee ML, et al. The retinal vasculature as a fractal: methodology, reliability, and relationship to blood pressure. Ophthalmology. 2008;115:1951–6.

  31. 31.

    Hart WE, Goldbaum M, Cote B, Kube P, Nelson MR. Measurement and classification of retinal vascular tortuosity. Int J Med Inform. 1999;53:239–52.

  32. 32.

    Zamir M, Medeiros JA, Cunningham TK. Arterial bifurcations in the human retina. J Gen Physiol. 1979;74:537–48.

  33. 33.

    Bray GA, Fruhbeck G, Ryan DH, Wilding JP. Management of obesity. Lancet. 2016;387:1947–56.

  34. 34.

    Johnson BL, Blackhurst DW, Latham BB, Cull DL, Bour ES, Oliver TL, et al. Bariatric surgery is associated with a reduction in major macrovascular and microvascular complications in moderately to severely obese patients with type 2 diabetes mellitus. J Am Coll Surg. 2013;216:545–56. discussion556-8

  35. 35.

    Shankar A, Sabanayagam C, Klein BE, Klein R. Retinal microvascular changes and the risk of developing obesity: population-based cohort study. Microcirculation. 2011;18:655–62.

  36. 36.

    Wong TY, Shankar A, Klein R, Klein BE, Hubbard LD. Prospective cohort study of retinal vessel diameters and risk of hypertension. BMJ. 2004;329:79.

  37. 37.

    Gishti O, Jaddoe VW, Felix JF, Klaver CC, Hofman A, Wong TY, et al. Retinal microvasculature and cardiovascular health in childhood. Pediatrics. 2015;135:678–85.

  38. 38.

    Hughes AD, Stanton AV, Jabbar AS, Chapman N, Martinez-Perez ME. and Mc GTSA. Effect of antihypertensive treatment on retinal microvascular changes in hypertension. J Hypertens. 2008;26:1703–7.

  39. 39.

    Dahlof B, Stenkula S, Hansson L. Hypertensive retinal vascular changes: relationship to left ventricular hypertrophy and arteriolar changes before and after treatment. Blood Press. 1992;1:35–44.

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Acknowledgements

This study was conducted within the Finnish Centre of Excellence in Cardiovascular and Metabolic Diseases supported by the Academy of Finland, the University of Turku, the Turku University Hospital, the Åbo Academy University, and the Finnish Eye Foundation.

Author information

Correspondence to Robyn J. Tapp.

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Conflict of interest

We declare that we have no conflicts of interest. This study was conducted within the Finnish Centre of Excellence in Cardiovascular and Metabolic Diseases supported by the Academy of Finland, the University of Turku, the Turku University Hospital, the Åbo Academy University, and the Finnish Eye Foundation. This study was registered at ClinicalTrials.gov under registration number NCT01373892.

Additional information

Synopsis

Bariatric surgery led to a reduction in retinal arteriolar narrowing and venular widening, with no changes observed in the control group. These findings are consistent with the observed cardiovascular risk reduction post bariatric surgery.

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Viljanen, A., Soinio, M., Cheung, C.Y. et al. Effects of bariatric surgery on retinal microvascular architecture in obese patients. Int J Obes 43, 1675–1680 (2019). https://doi.org/10.1038/s41366-018-0242-7

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