healthcareЗдравоохранение. HealthcareHealthcare1027-7218Republican Scientific and Practical Center for Medical Technologies, Informatization, Management and Health Economics10.65249/1027-7218-2026-2-4-11healthcare-246Research ArticleНАУЧНЫЕ ИССЛЕДОВАНИЯSCIENTIFIC RESEARCHПоказатели гликемической вариабельности, ассоциированные с диабетической ретинопатией, у пациентов с сахарным диабетом 2-го типаGlycemic variability indices associated with diabetic retinopathy in patients with type 2 diabetes mellitushttps://orcid.org/0009-0005-4501-6254СидоровичА. Р.SidorovichA.

Сидорович Анна Рышардовна – врач-офтальмолог отделения лазерной микрохирургии 

Ул. Уборевича, 73, 220096, г. Минск

https://orcid.org/0000-0002-9353-8664ИмшенецкаяТ. А.ImshenetskayaT.

Минск

https://orcid.org/0000-0003-0560-8843ДаниловаЛ. И.DanilovaL.

Минск

https://orcid.org/0009-0009-0876-1721ЗаборовскийИ. Г.ZaborovskyI.

Минск

https://orcid.org/0009-0004-5549-6645СавичВ. В.SavichV.

Минск

https://orcid.org/0009-0002-2370-5751РадьковаС. В.RadkovaS.

Минск

10-я городская клиническая больницаBelarusИнститут повышения квалификации и переподготовки кадров здравоохранения УО «Белорусский государственный медицинский университет»Belarus20261603202602411Copyright © Сидорович А.Р., Имшенецкая Т.А., Данилова Л.И., Заборовский И.Г., Савич В.В., Радькова С.В., 20262026Сидорович А.Р., Имшенецкая Т.А., Данилова Л.И., Заборовский И.Г., Савич В.В., Радькова С.В.Sidorovich A., Imshenetskaya T., Danilova L., Zaborovsky I., Savich V., Radkova S.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://healthcare.ejournal.by/jour/article/view/246Цель исследования

Цель исследования. Изучить показатели краткосрочной и долгосрочной вариабельности гликемии как факторы, связанные с диабетической ретинопатией, ее тяжестью и прогрессированием диабетической ретинопатии у пациентов с сахарным диабетом 2-го типа.

Материал и методы

Материал и методы. Проведен ретроспективный анализ 593 амбулаторных карт пациентов с сахарным диабетом 2-го типа (419 женщин (70,66 %) и 174 (29,32 %) мужчины, продолжительность заболевания – 10 [6; 15] лет), проходивших офтальмологическое обследование в отделении лазерной микрохирургии УЗ «10-я городская клиническая больница» за период 2016–2023 гг. Диабетическая ретинопатия была отмечена у 165 пациентов, группу лиц без экссудативно-геморрагических проявлений составили 428 пациентов. Динамика прогрессирования заболевания была отслежена за 1 и 3 года. Рассчитаны показатели вариабельности гликемии: SD, СV, MAGE, TIR. Статистическую обработку данных осуществляли с использованием пакета прикладных программ Statistica 12.

Результаты

Результаты. Установлен порог вариабельности гликемии (SD = 0,854, MAGE = 0,967) для определения наличия диабетической ретинопатии. Показатели SD и МАGE были статистически значимо выше у пациентов с данным заболеванием (1,253 [0,707; 1,893] vs 0,707 [0,283; 1,414], p = 0,021 и 1,4 [0,9; 2,3] vs 0,9 [0,4; 1,833], p = 0,021). Прогрессирование диабетической ретинопатии на первом году наблюдения было связано с более высокими показателями краткосрочной вариабельности гликемии: SD (3,8 [2,68; 4,9] vs 1,15 [0,71; 1,4], p = 0,045); CV (41,3 [35,37; 47,1] vs 15,71 [8,14; 16,0], p = 0,045); MAGE (4,9 [2,87; 7,0] vs 1,3 [1,0; 2,0], p = 0,045). Прогрессирование диабетической ретинопатии на третьем году наблюдения было ассоциировано с более высоким показателем долгосрочной вариабельности гликемии SD HbA1c (3,418 [3,042; 5,219] vs 0,202 [0,0; 0,52], p = 0,052).

Заключение

Заключение. Вариабельность гликемии была ассоциирована с наличием диабетической ретинопатии и ее прогрессированием, однако не может быть использована в качестве единственного маркера. Требуются дальнейшие исследования для установления комплекса показателей, эффективных для оценки риска прогрессирования заболевания.

Objective

Objective. To study short-term and long-term glycemic variability (GV) as factors associated with DR, its severity, and the progression of diabetic retinopathy in patients with type 2 diabetes mellitus.

Materials and methods

Materials and methods. A retrospective analysis was conducted of 593 patients with type 2 diabetes (419 women (70.66 %) and 174 men (29.32 %), disease duration 10 [6; 15] years) who underwent ophthalmological examination in the Laser Microsurgery Department of the City Clinical Hospital No. 10 for the period 2016-2023 was performed. DR was noted in 165 patients. The study included 428 patients without exudative-hemorrhagic manifestations. The dynamic of disease progression was monitored over a oneyear and three-year period. The GV SD, CV, MAGE, and TIR indices were calculated. Statistical data processing was performed using the Statistica 12 software package.

Results

Results. A GV SD threshold of 0.854 and MAGE 0.967 was established to detect the presence of DR. The SD and MAGE indices were statistically significantly higher in patients with DR (1.253 [0.707; 1.893] vs 0.707 [0.283; 1.414], p = 0.021 and 1.4 [0.9; 2.3] vs 0.9 [0.4; 1.833], p = 0.021). Progression of DR in the first year of observation was associated with higher rates of short-term GV SD (3.8 [2.68; 4.9] vs 1.15 [0.71; 1.4], p = 0.045); CV (41.3 [35.37; 47.1] vs 15.71 [8.14; 16.0], p = 0.045), MAGE (4.9 [2.87; 7.0] vs 1.3 [1.0; 2.0], p = 0.045). Progression of DR in the third year of observation was associated with higher rates of long-term GV SD HbA1c (3.418 [3.042; 5.219] vs 0.202 [0.0; 0.52], p = 0.052).

Conclusion

Conclusion. VG was associated with the presence of DR and its progression, but cannot be used as a sole marker. Further research is needed to establish a comprehensive set of markers that is effective in assessing the risk of DR progression.

диабетическая ретинопатияпрогнозирование прогрессированиясахарный диабетгликемиягликемическая вариабельностьdiabetic retinopathyprogression predictiondiabetes mellitusglycemiaglycemic variabilityReferencesIDF diabetes atlas // International diabetes federation. – 10th ed. – Brussels, 2021. – URL: https://www.diabetesatlas.org (date of access: 14.11.2022).IDF diabetes atlas. 10th ed. International diabetes federation. Brussels. 2021. Available at: https://www.diabetesatlas.org (accessed: 14.11.2022).Fundus photographic risk factors for progression of diabetic retinopathy ETDRS report number 12 / Early Treatment Diabetic Retinopathy Study Research Group // Journal of VitreoRetinal Diseases. Ophthalmology. – 1991. – Vol. 9, № 5. – P. 823–833.Early Treatment Diabetic Retinopathy Study Research Group. Fundus photographic risk factors for progression of diabetic retinopathy ETDRS. J VitreoRetin Dis. 1991; 9(5): 823–833.Assessing the importance of risk factors for diabetic retinopathy in patients with type 2 diabetes mellitus : results from the classification and regression tree models / Z. Zhang, D. Lv, Y. You [et al.] // Journal of family & community medicine. – 2024. – Vol. 31, № 3. – P. 197–205.Zhang Z., Lv D., You Y., et al. Assessing the importance of risk factors for diabetic retinopathy in patients with type 2 diabetes mellitus: results from the classification and regression tree models. J Family Community Med. 2024; 31(3): 197–205.Rapid reduction of HbA1c and early worsening of diabetic retinopathy : a real-world population-based study in subjects with type 2 diabetes / R. Simo, J. Franch-Nadal, B. Vlacho [et al.] // Diabetes Care. – 2023. – Vol. 46, № 9. – P. 1633–1639.Simo R., Franch-Nadal J., Vlacho B., et al. Rapid reduction of HbA1c and early worsening of Diabetic Retinopathy. Diabetes Care. 2023; 46(9): 1633–1639.Diabetic retinopathy environment-wide association study (EWAS) in NHANES 2005–2008 / K. Blighe, S. Gurudas, Y. Lee, S. Sivaprasad // Journal of clinical medicine. – 2020. – № 9. – P. 2005–2008.Blighe K., Gurudas S., Lee Y., Sivaprasad S. Diabetic retinopathy environment-wide association study (EWAS) in NHANES 2005– 2008. J Clin Med. 2020; 9: 2005–2008.The prevalence and systemic risk factors of diabetic macular edema : a cross-sectional study from Turkey / D. Acan, M. Calan, D. Er [et al.] // BMC Ophthalmology. – 2018. – № 18. – doi: 10.1186/s12886-018-0753-y.Acan D., Calan M., Er D., et al. The prevalence and systemic risk factors of diabetic macular edema. BMC Ophthalmol. 2018; 18. doi: 10.1186/s12886-018-0753-y.Long-term visit-to-visit glycemic variability as predictor of micro- and macrovascular complications in patients with type 2 diabetes: the Rio de Janeiro type 2 diabetes cohort study / C. R. L. Cardoso, N. C. Leite, C. B. M. Moram, G. F. Salles // Cardiovascular Diabetology. – 2018. – № 17. – doi: 10.1186/s12933-018-0677-0.Cardoso C.R.L., Leite N.C., Moram C.B.M., Salles G.F. Long-term visit-to-visit glycemic variability as predictor of micro- and macrovascular complications in patients with type 2 diabetes. Cardiovascular. Diabetol. 2018; 17. doi: 10.1186/s12933-018-0677-0.How to Measure Glycemic Variability? A Literature Review / S. Lazar, I. Ionita, D. Reurean-Pintilei, B. Timar // Medicina. – 2024. – Vol. 60 (1). – doi: 10.3390/medicina60010061.Lazar S., Ionita I., Reurean-Pintilei D., Timar B. How to Measure Glycemic Variability? Medicina. 2024; 60(1). doi: 10.3390/medicina60010061.Porta, M. Screening for diabetic retinopathy in Europe / M. Porta, E. M. Kohner // Diabetic Medicine. – 1991. – Vol. 8. – P. 197–198.Porta M., Kohner E.M. Screening for diabetic retinopathy in Europe. Diabetic Medicine. 1991; 8: 197–198.Glycemic profile variability as an independent predictor of diabetic retinopathy in patients with type 2 diabetes : a prospective cohort study / F. Dehghani Firouzabadi, A. Poopak, S. Samimi [et al.] // Frontiers in endocrinology (Lausanne). – 2024. – Vol. 7, № 15. – doi: 10.3389/fendo.2024.1383345Dehghani Firouzabadi F., Poopak A., Samimi S., et al. Glycemic profile variability as an independent predictor of diabetic retinopathy in patients with type 2 diabetes. Front Endocrinol (Lausanne). 2024; 7(15). doi: 10.3389/fendo.2024.1383345.Fasting glucose variation predicts microvascular risk in ACCORD and VADT / J. J. Zhou, J. Koska, G. Bahn, P. Reaven // The Journal of clinical endocrinology and metabolism. – 2021. – Vol. 106, № 4. – P. 1150–1162.Zhou J.J., Koska J., Bahn G., Reaven P. Fasting glucose variation predicts microvascular risk in ACCORD and VADT. J Clin Endocrinol Metab. 2021; 106(4): 1150–1162.Long-term outcomes among young adults with type 2 diabetes based on durability of glycemic control. Results from the today cohort study / Today study group // Diabetes care. – 2022. – Vol. 45, № 11. – P. 2689–2697.Today study group. Long-term outcomes among young adults with type 2 diabetes based on durability of glycemic control. Diabetes care. 2022; 45(11): 2689–2697.Glycemic variability assessed by continuous glucose monitoring and the risk of diabetic retinopathy in latent autoimmune diabetes of the adult and type 2 diabetes / J. Lu, X. Ma, L. Zhang [et al.] // Journal of diabetes investigation. – 2019. – Vol. 10, № 3. – P.753–759.Lu J., Ma X., Zhang L., et al. Glycemic variability assessed by continuous glucose monitoring and the risk of diabetic retinopathy in latent autoimmune diabetes of the adult and type 2 diabetes. Diabetes Invest. 2019; 10(3): 753–759.Relationship between Time in Range, Glycemic Variability, HbA1c, and complications in adults with type 1 diabetes Mellitus / A. El, M. Van Elsen, S. Charleer [et al.] // The Journal of clinical endocrinology and metabolism. – 2022. – Vol. 107, № 2. – P. 570–581.El A., Van Elsen M., Charleer S., et al. Relationship between Time in Range, Glycemic Variability, HbA1c, and complications in adults with type 1 diabetes Mellitus. J Clin Endocrinol Metab. 2022; 107(2): 570–581.Visit-to-visit variability of glycemia and vascular complications: the Hoorn Diabetes Care System cohort / R. C. Slieker, A. A. W. H. van der Heijden, G. Nijpels [et al.] // Cardiovascular diabetology. – 2019. – Vol. 18, № 1170. – doi: 10.1186/s12933-019-0975-1.Slieker R.C., H van der Heijden A. A. W. H., Nijpels G., et al. Visit-to-visit variability of glycemia and vascular complications. Cardiovasc Diabetol. 2019; 18. doi: 10.1186/s12933-019-0975-1.Hsieh, Y. T. Fasting plasma glucose variability is an independent risk factor for diabetic retinopathy and diabetic macular edema in type 2 diabetes : an 8-year prospective cohort study / Y. T. Hsieh, M. C. Hsieh // Clinical & experimental ophthalmology. – 2020. – Vol. 48, № 4. – P. 470–476.Hsieh Y.T., Hsieh M.C. Fasting plasma glucose variability is an independent risk factor for diabetic retinopathy and diabetic macular edema in type 2 diabetes. Clin Exp Ophthalmol. 2020; 48(4): 470–476.The Association between Mean glycated haemoglobin or glycaemic variability and the development of retinopathy in people with diabetes : a retrospective observational cohort study / K. Dhatariya, A. Humberstone, A. Hasnat [et al.] // Diabetes therapy: research, treatment and education of diabetes and related disorders. – 2021. – Vol. 12, № 10. – P. 2755–2766.Dhatariya K., Humberstone A., Hasnat A., et al. The Association between Mean glycated haemoglobin or glycaemic variability and the development of retinopathy in people with diabetes. Diabetes Therapy. 2021; 12(10): 2755–2766.Association between visit-to-visit variability of glycated albumin and diabetic retinopathy among patients with type 2 diabetes : a prospective cohort study / D. Dai, Y. Shen, J. Lu [et al.] // Journal of diabetes and its complications. – 2021. – Vol. 35, № 9. – doi: 10.1016/j.jdiacomp.2021.107971.Dai D., Shen Y., Lu J., et al. Association between visit-to-visit variability of glycated albumin and diabetic retinopathy among patients with type 2 diabetes. J Diabetes Complicat. 2021; 35(9). doi: 10.1016/j.jdiacomp.2021.107971.Kim, H.U. Long-term HbA1c variability and the development and progression of diabetic retinopathy in subjects with type 2 diabetes / H. U. Kim, S. P. Park, Y. K. Kim // Scientific reports. – 2021. – Vol. 11. – doi: 10.1038/s41598-021-84150-8.Kim H.U., Park S., Kim Y.K. Long-term HbA1c variability and the development and progression of diabetic retinopathy in subjects with type 2 diabetes. Sci Rep. 2021; 11. doi: 10.1038/s41598-021-84150-8.International Consensus on Use of continuous glucose monitoring / T. Danne, R. Nimri, T. Battelino [et al.] // Diabetes Care. – 2017. – Vol. 40, № 12. – P. 1631–1640.Danne T., Nimri R., Battelino T., et al. International Consensus on Use of continuous glucose monitoring. Diabetes Care. 2017; 40(12): 1631–1640.Defining the target value of the coefficient of variation by continuous glucose monitoring in Chinese people with diabetes / Y. Mo, X. Ma, J. Lu [et al.] // Journal of diabetes investigation. – 2021. – Vol. 12, № 6. – P. 1025–1034.Mo Y., Ma X., Lu J., et al. Defining the target value of the coefficient of variation by continuous glucose monitoring in Chinese people with diabetes. J Diabetes Invest. 2021; 12(6): 1025–1034.Monnier, L. Glycemic variability: the third component of the dysglycemia in diabetes. Is it important? How to measure it? / L. Monnier, C. Colette, D. R.Owens // Journal of Diabetes Science and Technology. – 2008. – Vol. 2, № 6. – P. 1094–1100.Monnier L., Colette C., Owens D.R. Glycemic variability: the third component of the dysglycemia in diabetes. Is it important? How to measure it? J Diabetes Sci Technol. 2008; 2 (6): 1094–1100.Comparison of glucose time in range and area under curve in range in relation to risk of diabetic retinopathy in type 2 diabetes patients / Y. Wang, J. Lu, Y. Shen [et al.] // Journal of diabetes investigation. – 2022. – Vol. 13, № 9. – P. 1543–1550.Wang Y., Lu J., Shen Y., et al. Comparison of glucose time in range and area under curve in range in relation to risk of diabetic retinopathy in type 2 diabetes patients. J Diabetes Investig. 2022; 13(9); 1543–1550.HbA1c variability and long-term glycemic control are linked to diabetic retinopathy and glomerular filtration rate in patients with type 1 diabetes and multiethnic background / L. Rosa, L. Zajdenverg, D. Lopes Souto [et al.] // Journal of diabetes and its complications. – 2019. – Vol. 33, № 9. – P. 610–615.Rosa L., Zajdenverg L., Lopes Souto D., et al. HbA1c variability and long-term glycemic control are linked to diabetic retinopathy and glomerular filtration rate in patients with type 1 diabetes and multiethnic background. J Diabetes Complicat. 2019; 33(9): 610–615.Mao, Y. HbA1c variability as an independent risk factor for microvascular complications in type 1 diabetes / Y. Mao, W. Zhong // Journal of diabetes science and technology. – 2024. – Vol. 18, № 2. – P. 380–388.Mao Y., Zhong W. HbA1c variability as an independent risk factor for microvascular complications in type 1 diabetes. J Diabetes Sci Technol. 2024; 18(2): 380–388.Effects of glycemic variability on the progression of diabetic retinopathy among patients with type 2 diabetes // J. Y. Park, J. H. Hwang, M. J. Kang [et al.] // Retina. – 2021. – Vol. 41, № 7. – P. 1487–1495.Park J.Y., Hwang J.H., Kang M.J., et al. Effects of glycemic variability on the progression of diabetic retinopathy among patients with type 2 diabetes. Retina. 2021; 41(7): 1487–1495.

The authors declare that there are no conflicts of interest present.