Modern strategies of alternative insulin delivery systems

Authors

DOI:

https://doi.org/10.14739/2310-1210.2023.3.274844

Keywords:

diabetes mellitus, oral drug administration, insulins

Abstract

There are barriers to initiation, use or intensification of insulin therapy for patients with diabetes. A non-invasive therapeutic approach in insulin therapy should overcome these barriers. The development of alternative methods of insulin delivery is a complex task of fundamental medicine and pharmacy. The availability of oral / nasal insulin helps millions of people with diabetes avoid daily burden of subcutaneous insulin injections.

The aim of the work was to study the current state of the latest developments in alternative routes of insulin delivery, their technology, and clinical trials.

Materials and methods. The latest publications of scientific research on non-invasive insulin delivery systems were the study objects. Content analysis, bibliosemantic, analytical, summarizing analyzes were used.

Results. The smart insulin delivery systems and pain-reducing technologies have been developed over the years. For this, research was conducted on numerous materials and technologies, including nanoparticles, hydrogels, liposomes, ionic liquids or special devices.

Several alternative delivery technologies have been identified to reduce pain (pain-reducing technologies): oral, inhaled, intranasal, buccal, transdermal, and long-acting injectable insulins, but with low frequency of use. Various modern technological approaches are applying, namely, chemical modification of insulin; mucoadhesion system; protease inhibitors; increased absorption; particle delivery systems. Smart insulin delivery technologies are based on different strategies, materials, and glucose-responsive synthesis and conversion, but a common “diffuse-type” insulin release mechanism is used. Innovations in insulin chemistry and formulations have shown improved clinical outcomes when used.

Conclusions. Innovations in alternative insulin delivery systems include algorithms for continuous glucose monitoring systems, glucose-sensitive polymer matrices and biological structures with insulin. The introduction of non-invasive systems would contribute to an earlier start of insulin therapy on medical advice, ensuring better glycemic control and reducing the risk of complications, which are the main burden on the health care system. The use of insulin in the form of alternative delivery systems may also be promising in the prevention of type 1 diabetes and other diseases.

Author Biographies

І. О. Vlasenko, Shupyk National Healthcare University of Ukraine, Kyiv

PhD, Associate Professor of the Department of Pharmaceutical Technology and Biopharmacy

L. L. Davtian, Shupyk National Healthcare University of Ukraine, Kyiv

PhD, DSc, Professor, Head of the Department of Pharmaceutical Technology and Biopharmaceutics

V. V. Hladyshev, Zaporizhzhia State Medical and Pharmaceutical University, Ukraine

PhD, DSc, Professor, Head of the Department of Medicines Technology

References

  1. International Diabetes Federation. (2021). Diabetes Atlas, (10th ed.). https://www.diabetesatlas.org
  2. Banting, F. G. (1925). Diabetes and insulin: Nobel lecture. https://www.nobelprize.org/prizes/medicine/1923/banting/lecture/
  3. Home, P. (2021). The evolution of insulin therapy. Diabetes research and clinical practice, 175, 108816. https://doi.org/10.1016/j.diabres.2021.108816
  4. Bhutta, Z. A., Salam, R. A., Gomber, A., Lewis-Watts, L., Narang, T., Mbanya, J. C., & Alleyne, G. (2021). A century past the discovery of insulin: global progress and challenges for type 1 diabetes among children and adolescents in low-income and middle-income countries. Lancet, 398(10313), 1837-1850. https://doi.org/10.1016/S0140-6736(21)02247-9
  5. Drucker, D. J. (2021). Transforming type 1 diabetes: the next wave of innovation. Diabetologia, 64(5), 1059-1065. https://doi.org/10.1007/s00125-021-05396-5
  6. Wright, A., Burden, A. C., Paisey, R. B., Cull, C. A., Holman, R. R., & U.K. Prospective Diabetes Study Group (2002). Sulfonylurea inadequacy: efficacy of addition of insulin over 6 years in patients with type 2 diabetes in the U.K. Prospective Diabetes Study (UKPDS 57). Diabetes care, 25(2), 330-336. https://doi.org/10.2337/diacare.25.2.330
  7. Turchin, A., Hosomura, N., Zhang, H., Malmasi, S., & Shubina, M. (2020). Predictors and consequences of declining insulin therapy by individuals with type 2 diabetes. Diabetic medicine, 37(5), 814-821. https://doi.org/10.1111/dme.14260
  8. Hendrieckx, C., Halliday, J. A., Beeney, L. J., & Speight, J. (2019). Diabetes and emotional health: a practical guide for healthcare professionals supporting adults with Type 1 and Type 2 diabetes, (2nd ed.) London: Diabetes UK. https://www.diabetes.org.uk/resources-s3/2019-03/0506%20Diabetes%20UK%20Australian%20Handbook_P4_FINAL_1.pdf
  9. Sood, A., & Panchagnula, R. (2001). Peroral route: an opportunity for protein and peptide drug delivery. Chemical reviews, 101(11), 3275-3303. https://doi.org/10.1021/cr000700m
  10. Raghavendran, S., Inbaraj, L. R., & Norman, G. (2020). Reason for refusal of insulin therapy among type 2 diabetes mellitus patients in primary care clinic in Bangalore. Journal of family medicine and primary care, 9(2), 854-858. https://doi.org/10.4103/jfmpc.jfmpc_973_19
  11. Truong, T. H., Nguyen, T. T., Armor, B. L., & Farley, J. R. (2017). Errors in the Administration Technique of Insulin Pen Devices: A Result of Insufficient Education. Diabetes therapy : research, treatment and education of diabetes and related disorders, 8(2), 221-226. https://doi.org/10.1007/s13300-017-0242-y
  12. NCD Risk Factor Collaboration (NCD-RisC) (2016). Worldwide trends in diabetes since 1980: a pooled analysis of 751 population-based studies with 4.4 million participants. Lancet, 387(10027), 1513-1530. https://doi.org/10.1016/S0140-6736(16)00618-8
  13. Brayden, D. (2021). The Centenary of the Discovery of Insulin: An Update on the Quest for Oral Delivery. Frontiers in Drug Delivery, 1, 726675. https://doi.org/10.3389/fddev.2021.726675
  14. Chatterjee, S., Bhushan Sharma, C., Lavie, C. J., Adhikari, A., Deedwania, P., & O'keefe, J. H. (2020). Oral insulin: an update. Minerva endocrinologica, 45(1), 49-60. https://doi.org/10.23736/S0391-1977.19.03055-4
  15. Chan, J., & Cheng-Lai, A. (2017). Inhaled Insulin: A Clinical and Historical Review. Cardiology in review, 25(3), 140-146. https://doi.org/10.1097/CRD.0000000000000143
  16. Setji, T. L., Hong, B. D., & Feinglos, M. N. (2016). Technosphere insulin: inhaled prandial insulin. Expert opinion on biological therapy, 16(1), 111-117. https://doi.org/10.1517/14712598.2016.1121230
  17. Dovc, K., & Battelino, T. (2020). Evolution of Diabetes Technology. Endocrinology and metabolism clinics of North America, 49(1), 1-18. https://doi.org/10.1016/j.ecl.2019.10.009
  18. Cernea, S., & Raz, I. (2020). Insulin Therapy: Future Perspectives. American journal of therapeutics, 27(1), e121-e132. https://doi.org/10.1097/MJT.0000000000001076
  19. Rege, N. K., Phillips, N. F. B., & Weiss, M. A. (2017). Development of glucose-responsive 'smart' insulin systems. Current opinion in endocrinology, diabetes, and obesity, 24(4), 267-278. https://doi.org/10.1097/MED.0000000000000345
  20. Halberg, I. B., Lyby, K., Wassermann, K., Heise, T., Zijlstra, E., & Plum-Mörschel, L. (2019). Efficacy and safety of oral basal insulin versus subcutaneous insulin glargine in type 2 diabetes: a randomised, double-blind, phase 2 trial. The lancet. Diabetes & endocrinology, 7(3), 179-188. https://doi.org/10.1016/S2213-8587(18)30372-3
  21. Easa, N., Alany, R. G., Carew, M., & Vangala, A. (2019). A review of non-invasive insulin delivery systems for diabetes therapy in clinical trials over the past decade. Drug discovery today, 24(2), 440-451. https://doi.org/10.1016/j.drudis.2018.11.010
  22. Seaquist, E. R., Blonde, L., McGill, J. B., Heller, S. R., Kendall, D. M., Bumpass, J. B., Pompilio, F. M., & Grant, M. L. (2020). Hypoglycaemia is reduced with use of inhaled Technosphere® Insulin relative to insulin aspart in type 1 diabetes mellitus. Diabetic medicine, 37(5), 752-759. https://doi.org/10.1111/dme.14202
  23. Nuffer, W., & Trujillo, J. (2016). The Role of Inhaled Insulin in the Management of Type 2 Diabetes. Pharmacology & Pharmacy, 07(04), 162-169. https://doi.org/10.4236/pp.2016.74021
  24. Hallschmid M. (2021). Intranasal insulin. Journal of neuroendocrinology, 33(4), e12934. https://doi.org/10.1111/jne.12934
  25. Caffarel-Salvador, E., Kim, S., Soares, V., Tian, R. Y., Stern, S. R., Minahan, D., Yona, R., Lu, X., Zakaria, F. R., Collins, J., Wainer, J., Wong, J., McManus, R., Tamang, S., McDonnell, S., Ishida, K., Hayward, A., Liu, X., Hubálek, F., Fels, J., … Traverso, G. (2021). A microneedle platform for buccal macromolecule delivery. Science advances, 7(4), eabe2620. https://doi.org/10.1126/sciadv.abe2620
  26. Rosenstock, J., Bajaj, H. S., Janež, A., Silver, R., Begtrup, K., Hansen, M. V., Jia, T., Goldenberg, R., & NN1436-4383 Investigators (2020). Once-Weekly Insulin for Type 2 Diabetes without Previous Insulin Treatment. The New England journal of medicine, 383(22), 2107-2116. https://doi.org/10.1056/NEJMoa2022474
  27. Shah, R. B., Patel, M., Maahs, D. M., & Shah, V. N. (2016). Insulin delivery methods: Past, present and future. International journal of pharmaceutical investigation, 6(1), 1-9. https://doi.org/10.4103/2230-973X.176456
  28. Rasmussen, C. H., Røge, R. M., Ma, Z., Thomsen, M., Thorisdottir, R. L., Chen, J. W., Mosekilde, E., & Colding-Jørgensen, M. (2014). Insulin aspart pharmacokinetics: an assessment of its variability and underlying mechanisms. European journal of pharmaceutical sciences, 62, 65-75. https://doi.org/10.1016/j.ejps.2014.05.010
  29. Souto, E. B., Souto, S. B., Campos, J. R., Severino, P., Pashirova, T. N., Zakharova, L. Y., Silva, A. M., Durazzo, A., Lucarini, M., Izzo, A. A., & Santini, A. (2019). Nanoparticle Delivery Systems in the Treatment of Diabetes Complications. Molecules, 24(23), 4209. https://doi.org/10.3390/molecules24234209
  30. Chen, Z., Han, S., Yang, X., Xu, L., Qi, H., Hao, G., Cao, J., Liang, Y., Ma, Q., Zhang, G., & Sun, Y. (2020). Overcoming Multiple Absorption Barrier for Insulin Oral Delivery Using Multifunctional Nanoparticles Based on Chitosan Derivatives and Hyaluronic Acid. International journal of nanomedicine, 15, 4877-4898. https://doi.org/10.2147/IJN.S251627
  31. Ge, L., You, X., Zhang, Y., Huang, K., Lu, X., Ren, Y., Zhu, Y., Dhinakar, A., Wu, J., & Qian, H. (2017). Development of self-emulsifying nanoplatform as anti-diabetic sulfonylurea carrier for oral diabetes therapy. Journal of Biomedical Nanotechnology, 13(8), 931-945. https://doi.org/10.1166/jbn.2017.2385
  32. Al Rubeaan, K., Rafiullah, M., & Jayavanth, S. (2016). Oral insulin delivery systems using chitosan-based formulation: a review. Expert opinion on drug delivery, 13(2), 223-237. https://doi.org/10.1517/17425247.2016.1107543
  33. Li, L., Jiang, G., Yu, W., Liu, D., Chen, H., Liu, Y., Huang, Q., Tong, Z., Yao, J., & Kong, X. (2016). A composite hydrogel system containing glucose-responsive nanocarriers for oral delivery of insulin. Materials science & engineering. C, Materials for biological applications, 69, 37-45. https://doi.org/10.1016/j.msec.2016.06.059
  34. Sun, Q., Zhang, Z., Zhang, R., Gao, R., & McClements, D. J. (2018). Development of Functional or Medical Foods for Oral Administration of Insulin for Diabetes Treatment: Gastroprotective Edible Microgels. Journal of agricultural and food chemistry, 66(19), 4820-4826. https://doi.org/10.1021/acs.jafc.8b00233
  35. Gedawy, A., Martinez, J., Al-Salami, H., & Dass, C. R. (2018). Oral insulin delivery: existing barriers and current counter-strategies. The Journal of pharmacy and pharmacology, 70(2), 197-213. https://doi.org/10.1111/jphp.12852
  36. Jarosinski, M. A., Dhayalan, B., Rege, N., Chatterjee, D., & Weiss, M. A. (2021). 'Smart' insulin-delivery technologies and intrinsic glucose-responsive insulin analogues. Diabetologia, 64(5), 1016-1029. https://doi.org/10.1007/s00125-021-05422-6
  37. Primavera, R., Bellotti, E., Di Mascolo, D., Di Francesco, M., Wang, J., Kevadiya, B. D., De Pascale, A., Thakor, A. S., & Decuzzi, P. (2021). Insulin Granule-Loaded MicroPlates for Modulating Blood Glucose Levels in Type-1 Diabetes. ACS applied materials & interfaces, 13(45), 53618-53629. https://doi.org/10.1021/acsami.1c16768
  38. Feyzioğlu-Demir, E., Üzüm, Ö. B. & Akgöl, S. (2022). Swelling and diffusion behaviour of spherical morphological polymeric hydrogel membranes (SMPHMs) containing epoxy groups and their application as drug release systems. Polymer Bulletin, 79. https://doi.org/10.1007/s00289-022-04368-y
  39. Xie, H., Ma, X., Lin, W., Dong, S., Liu, Q., Chen, Y., & Gao, Q. (2021). Linear Dextrin as Potential Insulin Delivery System: Effect of Degree of Polymerization on the Physicochemical Properties of Linear Dextrin-Insulin Inclusion Complexes. Polymers, 13(23), 4187. https://doi.org/10.3390/polym13234187
  40. Li, C., Liu, X., Liu, Y., Huang, F., Wu, G., Liu, Y., Zhang, Z., Ding, Y., Lv, J., Ma, R., An, Y., & Shi, L., (2019). Glucose and H2O2 dual-sensitive nanogels for enhanced glucose-responsive insulin delivery. Nanoscale, 11(18), 9163-9175. https://doi.org/10.1039/c9nr01554j
  41. Chai, Z., Dong, H., Sun, X., Fan, Y., Wang, Y., & Huang, F. (2020). Development of glucose oxidase-immobilized alginate nanoparticles for enhanced glucose-triggered insulin delivery in diabetic mice. International journal of biological macromolecules, 159, 640-647. https://doi.org/10.1016/j.ijbiomac.2020.05.097
  42. Mohammadpour, F., Hadizadeh, F., Tafaghodi, M., Sadri, K., Mohammadpour, A. H., Kalani, M. R., Gholami, L., Mahmoudi, A., & Chamani, J. (2019). Preparation, in vitro and in vivo evaluation of PLGA/Chitosan based nano-complex as a novel insulin delivery formulation. International journal of pharmaceutics, 572, 118710. https://doi.org/10.1016/j.ijpharm.2019.118710
  43. Sarkar, S., Das, D., Dutta, P., Kalita, J., Wann, S. B., & Manna, P. (2020). Chitosan: A promising therapeutic agent and effective drug delivery system in managing diabetes mellitus. Carbohydrate polymers, 247, 116594. https://doi.org/10.1016/j.carbpol.2020.116594
  44. Matsumoto, A., Tanaka, M., Matsumoto, H., Ochi, K., Moro-Oka, Y., Kuwata, H., Yamada, H., Shirakawa, I., Miyazawa, T., Ishii, H., Kataoka, K., Ogawa, Y., Miyahara, Y., & Suganami, T. (2017). Synthetic "smart gel" provides glucose-responsive insulin delivery in diabetic mice. Science advances, 3(11), eaaq0723. https://doi.org/10.1126/sciadv.aaq0723
  45. Mohanty, A. R., Ravikumar, A., & Peppas, N. A. (2022). Recent advances in glucose-responsive insulin delivery systems: novel hydrogels and future applications. Regenerative biomaterials, 9, rbac056. https://doi.org/10.1093/rb/rbac056
  46. Farhoudi, N., Leu, H. Y., Laurentius, L. B., Magda, J. J., Solzbacher, F., & Reiche, C. F. (2020). Smart Hydrogel Micromechanical Resonators with Ultrasound Readout for Biomedical Sensing. ACS sensors, 5(7), 1882-1889. https://doi.org/10.1021/acssensors.9b02180
  47. Song, J., Zhang, Y., Chan, S. Y., Du, Z., Yan, Y., Wang, T., Li, P., & Huang, W. (2021). Hydrogel-based flexible materials for diabetes diagnosis, treatment, and management. Npj Flexible Electronics, 5, 26. https://doi.org/10.1038/s41528-021-00122-y
  48. Yu, J., Zhang, Y., Sun, W., Kahkoska, A. R., Wang, J., Buse, J. B., & Gu, Z. (2017). Insulin-Responsive Glucagon Delivery for Prevention of Hypoglycemia. Small, 13(19), 10.1002/smll.201603028. https://doi.org/10.1002/smll.201603028
  49. Culebras, M., Barrett, A., Pishnamazi, M., Walker, G. M., & Collins, M. N. (2021). Wood-Derived Hydrogels as a Platform for Drug-Release Systems. ACS sustainable chemistry & engineering, 9(6), 2515-2522. https://doi.org/10.1021/acssuschemeng.0c08022
  50. Zhang, Y., Zhou, W., Shen, L., Lang, L., Huang, X., Sheng, H., Ning, G., & Wang, W. (2022). Safety, Pharmacokinetics, and Pharmacodynamics of Oral Insulin Administration in Healthy Subjects: A Randomized, Double-Blind, Phase 1 Trial. Clinical pharmacology in drug development, 11(5), 606-614. https://doi.org/10.1002/cpdd.1060
  51. Hubálek, F., Refsgaard, H. H. F., Gram-Nielsen, S., Madsen, P., Nishimura, E., Münzel, M., Brand, C. L., Stidsen, C. E., Claussen, C. H., Wulff, E. M., Pridal, L., Ribel, U., Kildegaard, J., Porsgaard, T., Johansson, E., Steensgaard, D. B., Hovgaard, L., Glendorf, T., Hansen, B. F., Jensen, M. K., … Kjeldsen, T. (2020). Molecular engineering of safe and efficacious oral basal insulin. Nature communications, 11(1), 3746. https://doi.org/10.1038/s41467-020-17487-9
  52. Benyettou, F., Kaddour, N., Prakasam, T., Das, G., Sharma, S. K., Thomas, S. A., Bekhti-Sari, F., Whelan, J., Alkhalifah, M. A., Khair, M., Traboulsi, H., Pasricha, R., Jagannathan, R., Mokhtari-Soulimane, N., Gándara, F., & Trabolsi, A. (2021). In vivo oral insulin delivery via covalent organic frameworks. Chemical science, 12(17), 6037-6047. https://doi.org/10.1039/d0sc05328g
  53. Domokos, G., & Várkonyi, P. L. (2008). Geometry and self-righting of turtles. Proceedings. Biological sciences, 275(1630), 11-17. https://doi.org/10.1098/rspb.2007.1188
  54. Abramson, A., Caffarel-Salvador, E., Khang, M., Dellal, D., Silverstein, D., Gao, Y., Frederiksen, M. R., Vegge, A., Hubálek, F., Water, J. J., Friderichsen, A. V., Fels, J., Kirk, R. K., Cleveland, C., Collins, J., Tamang, S., Hayward, A., Landh, T., Buckley, S. T., Roxhed, N., … Traverso, G. (2019). An ingestible self-orienting system for oral delivery of macromolecules. Science, 363(6427), 611-615. https://doi.org/10.1126/science.aau2277
  55. Abramson, A., Frederiksen, M. R., Vegge, A., Jensen, B., Poulsen, M., Mouridsen, B., Jespersen, M. O., Kirk, R. K., Windum, J., Hubálek, F., Water, J. J., Fels, J., Gunnarsson, S. B., Bohr, A., Straarup, E. M., Ley, M. W. H., Lu, X., Wainer, J., Collins, J., Tamang, S., … Traverso, G. (2022). Oral delivery of systemic monoclonal antibodies, peptides and small molecules using gastric auto-injectors. Nature biotechnology, 40(1), 103-109. https://doi.org/10.1038/s41587-021-01024-0
  56. Eldor, R., Neutel, J., Homer, K., & Kidron, M. (2021). Efficacy and safety of 28-day treatment with oral insulin (ORMD-0801) in patients with type 2 diabetes: A randomized, placebo-controlled trial. Diabetes, obesity & metabolism, 23(11), 2529-2538. https://doi.org/10.1111/dom.14499
  57. Eldor, R., G. Fleming, A., Neutel, J., Homer, K. E., Kidron, M., & Rosenstock J. (2020). 105-LB: Evening Oral Insulin (ORMD-0801) Glycemic Effects in Uncontrolled T2DM Patients. Diabetes, 69(Supplement_1). https://doi.org/10.2337/db20-105-lb
  58. Zijlstra, E., Heinemann, L., & Plum-Mörschel, L. (2014). Oral insulin reloaded: a structured approach. Journal of diabetes science and technology, 8(3), 458-465. https://doi.org/10.1177/1932296814529988
  59. New Drug Approvals. (n.d.). OI 338. https://newdrugapprovals.org/2021/01/25/oi-338/
  60. Lansdowne, L. E., & Campbell, M. (2021, April 28). A Step Closer to Orally-Delivered Insulin for Diabetes. Technology Networks. Drug Delivery. https://www.technologynetworks.com/drug-discovery/articles/a-step-closer-to-orally-delivered-insulin-for-diabetes-348218
  61. Aquestive. (2020). Innovative Drug Delivery. https://aquestive.com/innovative-drug-delivery-pharmfilm/
  62. Harrison, L. C. (2021). The dark side of insulin: A primary autoantigen and instrument of self-destruction in type 1 diabetes. Molecular metabolism, 52, 101288. https://doi.org/10.1016/j.molmet.2021.101288
  63. Writing Committee for the Type 1 Diabetes TrialNet Oral Insulin Study Group, Krischer, J. P., Schatz, D. A., Bundy, B., Skyler, J. S., & Greenbaum, C. J. (2017). Effect of Oral Insulin on Prevention of Diabetes in Relatives of Patients With Type 1 Diabetes: A Randomized Clinical Trial. JAMA, 318(19), 1891-1902. https://doi.org/10.1001/jama.2017.17070
  64. Bonifacio, E., Ziegler, A. G., Klingensmith, G., Schober, E., Bingley, P. J., Rottenkolber, M., Theil, A., Eugster, A., Puff, R., Peplow, C., Buettner, F., Lange, K., Hasford, J., Achenbach, P., & Pre-POINT Study Group (2015). Effects of high-dose oral insulin on immune responses in children at high risk for type 1 diabetes: the Pre-POINT randomized clinical trial. JAMA, 313(15), 1541-1549. https://doi.org/10.1001/jama.2015.2928
  65. Zhang, Y., Yu, J., Kahkoska, A. R., Wang, J., Buse, J. B., & Gu, Z. (2019). Advances in transdermal insulin delivery. Advanced drug delivery reviews, 139, 51-70. https://doi.org/10.1016/j.addr.2018.12.006
  66. Vadlapatla, R., Wong, E. Y., & Gayakwad, S. G. (2017). Electronic drug delivery systems: Journal of Drug Delivery Science and Technology, 41, 359-366. https://doi.org/10.1016/j.jddst.2017.08.008
  67. Zhang, Y., Yu, J., Bomba, H. N., Zhu, Y., & Gu, Z. (2016). Mechanical Force-Triggered Drug Delivery. Chemical reviews, 116(19), 12536-12563. https://doi.org/10.1021/acs.chemrev.6b00369
  68. Bhatnagar, S., Dave, K., & Venuganti, V. V. K. (2017). Microneedles in the clinic. Journal of controlled release, 260, 164-182. https://doi.org/10.1016/j.jconrel.2017.05.029
  69. Jin, X., Zhu, D. D., Chen, B. Z., Ashfaq, M., & Guo, X. D. (2018). Insulin delivery systems combined with microneedle technology. Advanced drug delivery reviews, 127, 119-137. https://doi.org/10.1016/j.addr.2018.03.011
  70. Rzhevskiy, A. S., Singh, T. R. R., Donnelly, R. F., & Anissimov, Y. G. (2018). Microneedles as the technique of drug delivery enhancement in diverse organs and tissues. Journal of controlled release, 270, 184-202. https://doi.org/10.1016/j.jconrel.2017.11.048
  71. Larrañeta, E., McCrudden, M. T., Courtenay, A. J., & Donnelly, R. F. (2016). Microneedles: A New Frontier in Nanomedicine Delivery. Pharmaceutical research, 33(5), 1055-1073. https://doi.org/10.1007/s11095-016-1885-5
  72. Prausnitz, M. R. (2017). Engineering Microneedle Patches for Vaccination and Drug Delivery to Skin. Annual review of chemical and biomolecular engineering, 8, 177-200. https://doi.org/10.1146/annurev-chembioeng-060816-101514
  73. Gradel, A. K. J., Porsgaard, T., Lykkesfeldt, J., Seested, T., Gram-Nielsen, S., Kristensen, N. R., & Refsgaard, H. H. F. (2018). Factors Affecting the Absorption of Subcutaneously Administered Insulin: Effect on Variability. Journal of diabetes research, 2018, 1205121. https://doi.org/10.1155/2018/1205121
  74. Barclay, L. (2006, February 9). Exubera Approved Despite Initial Lung Function Concerns. Medscape. https://www.medscape.com/viewarticle/523294
  75. Khan, A. B., Ahmad, A., Ahmad, S., Gul, M., Iqbal, F., Ullah, H., Laiba, S., & Orakzai, U. K. (2022). Comparative Analysis of Inhaled Insulin With Other Types in Type 1 Diabetes Mellitus: A Systematic Review and Meta-Analysis. Cureus, 14(4), e23731. https://doi.org/10.7759/cureus.23731
  76. Annabestani, Z., Sharghi, S., Shahbazi, S., Monfared, S., Karimi, F., Taheri, E., Heshmat, R., & Larijani, B. (2010). Insulin buccal spray (Oral-Lyn) efficacy in type 1 diabetes. Iranian Journal of Diabetes and Lipid Disorders, 9, 1-4.
  77. Nazar, H., Caliceti, P., Carpenter, B., El-Mallah, A. I., Fatouros, D. G., Roldo, M., van der Merwe, S. M., & Tsibouklis, J. (2013). A once-a-day dosage form for the delivery of insulin through the nasal route: in vitro assessment and in vivo evaluation. Biomaterials science, 1(3), 306-314. https://doi.org/10.1039/c2bm00132b
  78. Tashima, T. (2020). Shortcut Approaches to Substance Delivery into the Brain Based on Intranasal Administration Using Nanodelivery Strategies for Insulin. Molecules, 25(21), 5188. https://doi.org/10.3390/molecules25215188
  79. Novak, V., Mantzoros, C. S., Novak, P., McGlinchey, R., Dai, W., Lioutas, V., Buss, S., Fortier, C. B., Khan, F., Aponte Becerra, L., & Ngo, L. H. (2022). MemAID: Memory advancement with intranasal insulin vs. placebo in type 2 diabetes and control participants: a randomized clinical trial. Journal of neurology, 269(9), 4817-4835. https://doi.org/10.1007/s00415-022-11119-6

Downloads

Published

2023-05-31

How to Cite

1.
Vlasenko ІО, Davtian LL, Hladyshev VV. Modern strategies of alternative insulin delivery systems. Zaporozhye Medical Journal [Internet]. 2023May31 [cited 2026May15];25(3):262-9. Available from: https://zmj.zsmu.edu.ua/article/view/274844

Issue

Vol. 25 No. 3 (2023)

Section

Review

License

Authors who publish with this journal agree to the following terms:

Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.  Лицензия Creative Commons