Chitosan-based particulate systems for drug and vaccine delivery in the treatment and prevention of neglected tropical diseases

Abstract

Neglected tropical diseases (NTDs) are a diverse group of infections which are difficult to prevent or control, affecting impoverished communities that are unique to tropical or subtropical regions. In spite of the low number of drugs that are currently used for the treatment of these diseases, progress on new drug discovery and development for NTDs is still very limited. Therefore, strategies on the development of new delivery systems for current drugs have been the main focus of formulators to provide improved efficacy and safety. In recent years, particulate delivery systems at micro- and nanosize, including polymeric micro- and nanoparticles, liposomes, solid lipid nanoparticles, metallic nanoparticles, and nanoemulsions, have been widely investigated in the treatment and control of NTDs. Among these polymers used for the preparation of such systems is chitosan, which is a marine biopolymer obtained from the shells of crustaceans. Chitosan has been investigated as a delivery system due to the versatility of its physicochemical properties as well as bioadhesive and penetration-enhancing properties. Furthermore, chitosan can be also used to improve treatment due to its bioactive properties such as antimicrobial, tissue regeneration, etc. In this review, after giving a brief introduction to neglected diseases and particulate systems developed for the treatment and control of NTDs, the chitosan-based systems will be described in more detail and the recent studies on these systems will be reviewed.

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References

  1. 1.

    WHO-Department of control of neglected tropical diseases. A road map for neglected tropical diseases 2021–2030, ending the neglect to attain the sustainable development goals 2020; WHO/UCN/NTD/2020.01; WHO: Geneva. https://www.who.int/neglected_diseases/diseases/en/; (accessed on 20 March 2020).

  2. 2.

    WHO-Department of control of neglected tropical diseases. A road map for neglected tropical diseases 2021–2030, ending the neglect to attain the sustainable development goals 2020; WHO/UCN/NTD/2020.01; WHO: Geneva; 15 May 2020.

  3. 3.

    WHO. Global update on implementation of preventive chemotherapy against neglected tropical diseases in 2018. Wkly Epidemiol Rec. 2019;38(94):425–40.

    Google Scholar 

  4. 4.

    Date AA, Joshi MD, Patravale VB. Parasitic diseases: liposomes and polymeric nanoparticles versus lipid nanoparticles. Adv Drug Deliv Rev. 2007;59(6):505–21. https://doi.org/10.1016/j.addr.2007.04.009.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Islan GA, Durán M, Cacicedo ML, Nakazato G, Kobayashi RKT, Martinez DST, et al. Nanopharmaceuticals as a solution to neglected diseases: is it possible? Acta Trop. 2017;170:16–42. https://doi.org/10.1016/j.actatropica.2017.02.019.

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Romero EL, Morilla MJ. Nanotechnological approaches against Chagas disease. Adv Drug Deliv Rev. 2010;62(4–5):576–88. https://doi.org/10.1016/j.addr.2009.11.025.

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Akbari M, Oryan A, Hatam G. Application of nanotechnology in treatment of leishmaniasis: a review. Acta Trop. 2017;172:86–90. https://doi.org/10.1016/j.actatropica.2017.04.029.

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    De Souza A, Marins DSS, Mathias SL, Monteiro LM, Yukuyama MN, Scarim CB, et al. Promising nanotherapy in treating leishmaniasis. Int J Pharm. 2018;547(1–2):421–31. https://doi.org/10.1016/j.ijpharm.2018.06.018.

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Walvekar P, Gannimani R, Govender T. Combination drug therapy via nanocarriers against infectious diseases. Eur J Pharm Sci. 2019;127:121–41. https://doi.org/10.1016/j.ejps.2018.10.017.

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Pund S, Joshi A. Nanoarchitectures for neglected tropical protozoal diseases: challenges and state of the art. In: Grumezescu AM, editor. Nano- and microscale drug delivery systems: Elsevier; 2017;439–80. https://doi.org/10.1016/B978-0-323-52727-9.00023-6.

  11. 11.

    Rafati S, Gholami E, Zahedifard F. Delivery systems for Leishmania vaccine development. Expert Rev Vaccines. 2016;15(7):879–95. https://doi.org/10.1586/14760584.2016.1157478.

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Volpedo G, Costa L, Ryan N, Halsey G, Satoskar A, Oghumu S. Nanoparticulate drug delivery systems for the treatment of neglected tropical protozoan diseases. J Venom Anim Toxins. 2019;25. https://doi.org/10.1590/1678-9199-jvatitd-1441-18.

  13. 13.

    CDC. Buruli ulcer. https://www.cdc.gov/buruli-ulcer/index.html; (accessed on 20 March 2020).

  14. 14.

    WHO. Buruli ulcer (Mycobacterium ulcerans infection). https://www.who.int/news-room/fact-sheets/detail/buruli-ulcer-(mycobacterium-ulcerans-infection); (accessed on 20 March 2020).

  15. 15.

    WHO. Prevent dengue & chikungunya. WHO Myanmar newsletter special. 2019.

  16. 16.

    FDA. Dengvaxia. https://www.fda.gov/vaccines-blood-biologics/dengvaxia; (accessed on 20 March 2020).

  17. 17.

    CDC. Chagas disease. https://www.cdc.gov/parasites/chagas/; (accessed on 20 March 2020).

  18. 18.

    WHO. Chagas disease (American trypanosomiasis). https://www.who.int/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis); (accessed on 20 March 2020).

  19. 19.

    WHO. Dracunculiasis (guinea-worm disease). https://www.who.int/news-room/fact-sheets/detail/dracunculiasis-(guinea-worm-disease); (accessed on 20 March 2020).

  20. 20.

    WHO. Echinococcosis. https://www.who.int/news-room/fact-sheets/detail/echinococcosis; (accessed on 20 March 2020).

  21. 21.

    CDC. Parasites-echinococcosis. https://www.cdc.gov/parasites/echinococcosis/; (accessed on 20 March 2020).

  22. 22.

    WHO. Foodborne trematodiases. https://www.who.int/news-room/fact-sheets/detail/foodborne-trematodiases; (accessed on 20 March 2020).

  23. 23.

    WHO. Trypanosomiasis, human African (sleeping sickness). https://www.who.int/news-room/fact-sheets/detail/trypanosomiasis-human-african-(sleeping-sickness); (accessed on 20 March 2020).

  24. 24.

    WHO. Leishmaniasis. https://www.who.int/news-room/fact-sheets/detail/leishmaniasis; (accessed on 20 March 2020).

  25. 25.

    CDC. Leishmaniasis. https://www.cdc.gov/parasites/leishmaniasis/; (accessed on 20 March 2020).

  26. 26.

    WHO. Leprosy. https://www.who.int/news-room/fact-sheets/detail/leprosy; (accessed on 20 March 2020).

  27. 27.

    WHO. Leprosy elimination. https://www.who.int/lep/disease/treatment/en/; (accessed on 20 March 2020).

  28. 28.

    WHO. Lymphatic filariasis. https://www.who.int/news-room/fact-sheets/detail/lymphatic-filariasis; (accessed on 20 March 2020).

  29. 29.

    WHO. Mycetoma, chromoblastomycosis and other deep mycoses. https://www.who.int/neglected_diseases/diseases/mycetoma-chromoblastomycosis-deep-mycoses/en/; (accessed on 20 March 2020).

  30. 30.

    WHO. Onchocerciasis. https://www.who.int/news-room/fact-sheets/detail/onchocerciasis; (accessed on 20 March 2020).

  31. 31.

    WHO. Rabies. https://www.who.int/ith/vaccines/rabies/en/; (accessed on 20 March 2020).

  32. 32.

    WHO. Scabies and other ectoparasites. https://www.who.int/neglected_diseases/diseases/scabies-and-other-ectoparasites/en/; (accessed 24 March 2020).

  33. 33.

    CDC. Scabies medication. https://www.cdc.gov/parasites/scabies/health_professionals/meds.html; (accessed on 20 March 2020).

  34. 34.

    WHO. Schistosomiasis. https://www.who.int/news-room/fact-sheets/detail/schistosomiasis; (accessed on 20 March 2020).

  35. 35.

    CDC. Parasites - soil-transmitted helminths. https://www.cdc.gov/parasites/sth/index.html; (accessed on 20 March 2020).

  36. 36.

    WHO. Soil-transmitted helminth infections. https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections; (accessed on 20 March 2020).

  37. 37.

    WHO. Snakebite envenoming. https://www.who.int/snakebites/disease/en/; (accessed on 20 March 2020).

  38. 38.

    WHO. Taeniasis/cysticercosis. https://www.who.int/news-room/fact-sheets/detail/taeniasis-cysticercosis; (accessed on 20 March 2020).

  39. 39.

    WHO. Trachoma. https://www.who.int/news-room/fact-sheets/detail/trachoma; (accessed on 20 March 2020).

  40. 40.

    WHO. Yaws eradication. https://www.who.int/yaws/en/; (accessed on 20 March 2020).

  41. 41.

    Gregoriadis G, Florence AT. Liposomes in drug delivery. Drugs. 1993;45:15–28. https://doi.org/10.2165/00003495-199345010-00003.

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Akbarzadeh A, Rezaei-Sadabady R, Davaran S, Joo SW, Zarghami N, Hanifehpour Y, et al. Liposome: classification, preparation, and applications. Nanoscale Res Lett. 2013;8:102. https://doi.org/10.1186/1556-276x-8-102.

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Gregoriadis G, Perrie Y. Liposomes. In: Encyclopedia of Life Sciences (ELS). JohnWiley & Sons, Ltd: Chicheste; 2010r. https://doi.org/10.1002/9780470015902.a0002656.pub2.

  44. 44.

    Lovelyn C. Current state of nanoemulsions in drug delivery. JBNB. 2011;2:626–39. https://doi.org/10.4236/jbnb.2011.225075.

    CAS  Article  Google Scholar 

  45. 45.

    Jaiswal M, Dudhe R, Sharma PK. Nanoemulsion: an advanced mode of drug delivery system. 3 Biotech. 2015;5:123–7. https://doi.org/10.1007/s13205-014-0214-0.

    Article  PubMed  Google Scholar 

  46. 46.

    Aliabadi HM, Lavasanifar A. Polymeric micelles for drug delivery. Expert Opin Drug Deliv. 2006;3(1):139–62. https://doi.org/10.1517/17425247.3.1.139.

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Croy SR, Kwon GS. Polymeric micelles for drug delivery. Curr Pharm Des. 2006;12(36):4669–84. https://doi.org/10.2174/138161206779026245.

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Kumari A, Yadav SK, Yadav SC. Biodegradable polymeric nanoparticles based drug delivery systems. Colloids Surf B. 2010;75(1):1–18. https://doi.org/10.1016/j.colsurfb.2009.09.001.

    CAS  Article  Google Scholar 

  49. 49.

    Elsabahy M, Wooley KL. Design of polymeric nanoparticles for biomedical delivery applications. Chem Soc Rev. 2012;41(7):2545. https://doi.org/10.1039/c2cs15327k.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Banik BL, Fattahi P, Brown JL. Polymeric nanoparticles: the future of nanomedicine. WIREs Nanomed Nanobiotechnol. 2015;8:n/a-n/a. https://doi.org/10.1002/wnan.1364.

  51. 51.

    Arvizo RR, Bhattacharyya S, Kudgus RA, Giri K, Bhattacharya R, Mukherjee P. Intrinsic therapeutic applications of noble metal nanoparticles: past, present and future. Chem Soc Rev. 2012;41(7):2943. https://doi.org/10.1039/c2cs15355f.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Kazi KM, Mandal AS, Biswas N, Guha A, Chatterjee S, Behera M, et al. Niosome: a future of targeted drug delivery systems. J Adv Pharm Technol Res. 2010;1(4):374–80. https://doi.org/10.4103/0110-5558.76435.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Yadav N, Khatak S, Sara UVS. Solid lipid nanoparticles - a review. Int J App Pharm. 2013;5(2):8–18.

    CAS  Google Scholar 

  54. 54.

    Ghasemiyeh P, Mohammadi-Samani S. Solid lipid nanoparticles and nanostructured lipid carriers as novel drug delivery systems: applications, advantages and disadvantages. Res Pharm Sci. 2018;13(4):288–303. https://doi.org/10.4103/1735-5362.235156.

    Article  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Emerich DF, Thanos CG. Nanotechnology and medicine. Expert Opin Biol Ther. 2003;3(4):655–63. https://doi.org/10.1517/14712598.3.4.655.

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Duran N, Marcato PD, Teixeira Z, Duran M, Costa FTM, Brocchi M. State of the art of nanobiotechnology applications in neglected diseases. Curr Nanosci. 2009;5:396–408. https://doi.org/10.2174/157341309789378069.

    CAS  Article  Google Scholar 

  57. 57.

    Tomiotto-Pellissier F, Miranda-Sapla MM, Machado LF, Bortoleti BTDS, Sahd CS, Chagas AF, et al. Nanotechnology as a potential therapeutic alternative for schistosomiasis. Acta Trop. 2017;174:64–71. https://doi.org/10.1016/j.actatropica.2017.06.025.

    CAS  Article  PubMed  Google Scholar 

  58. 58.

    Shah A, Gupta SS. Anti-leishmanial nanotherapeutics: a current perspective. Curr Drug Metab. 2019;20(6):473–82. https://doi.org/10.2174/1389200219666181022163424.

    CAS  Article  PubMed  Google Scholar 

  59. 59.

    Sun Y, Chen D, Pan Y, Qu W, Hao H, Wang X, et al. Nanoparticles for antiparasitic drug delivery. Drug Deliv. 2019;26(1):1206–21. https://doi.org/10.1080/10717544.2019.1692968.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Singh M, Chakrapani A, O'Hagan D. Nanoparticles and microparticles as vaccine-delivery systems. Expert Rev Vaccines. 2007;6(5):797–808. https://doi.org/10.1586/14760584.6.5.797.

    CAS  Article  PubMed  Google Scholar 

  61. 61.

    De Temmerman ML, Rejman J, Demeester J, Irvine DJ, Gander B, De Smedt SC. Particulate vaccines: on the quest for optimal delivery and immune response. Drug Discov Today. 2011;16(13–14):569–82. https://doi.org/10.1016/j.drudis.2011.04.006.

    CAS  Article  PubMed  Google Scholar 

  62. 62.

    Lebre F, Hearnden CH, Lavelle EC. Modulation of immune responses by particulate materials. Adv Mater. 2016;28:5525–41 https://doi.org/10.1002/adma.201505395.

  63. 63.

    Roberts GAF. Chitin chemistry. New York: Macmillan Education; 1992.

    Google Scholar 

  64. 64.

    Peniche C, Argüelles-Monal W, Goycoolea FM. Chapter 25 - chitin and chitosan: major sources, properties and applications. In: Belgacem MN, Gandini A, editors. Monomers, polymers and composites from renewable resources. Amsterdam: Elsevier; 2008. p. 517–42.

    Google Scholar 

  65. 65.

    Younes I, Rinaudo M. Chitin and chitosan preparation from marine sources. Structure, properties and applications. Mar Drugs. 2015;13(3):1133–74. https://doi.org/10.3390/md13031133.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Roberts GAF. Thirty years of progress in chitin and chitosan. Prog Chem Appl Chitin. 2008;13:7–15 http://ptchit.lodz.pl/PTChit/13_01.pdf.

    Google Scholar 

  67. 67.

    Basa S, Nampally M, Honorato T, Das SN, Podile AR, El Gueddari NE, et al. The pattern of acetylation defines the priming activity of chitosan tetramers. J Am Chem Soc. 2020;142(4):1975–86. https://doi.org/10.1021/jacs.9b11466.

    CAS  Article  PubMed  Google Scholar 

  68. 68.

    Weinhold MX, Sauvageau JCM, Kumirska J, Thöming J. Studies on acetylation patterns of different chitosan preparations. Carbohydr Polym. 2009;78(4):678–84. https://doi.org/10.1016/j.carbpol.2009.06.001.

    CAS  Article  Google Scholar 

  69. 69.

    European Pharmacopoeia 9th edition: Monograph 1774; Council of European: Strasbourg, France; 2016.

  70. 70.

    The United States Pharmacopeia/The National Formulary 42/NF37; United States Pharmacopeial Convention: Rockville (MD); 2019: pp. 5663.

  71. 71.

    Şenel S. Current status and future of chitosan in drug and vaccine delivery. React Funct Polym. 2019;147:104452. https://doi.org/10.1016/j.reactfunctpolym.2019.104452.

    CAS  Article  Google Scholar 

  72. 72.

    Kean T, Roth S, Thanou M. Trimethylated chitosans as non-viral gene delivery vectors: cytotoxicity and transfection efficiency. J Control Release. 2005;103:643–53. https://doi.org/10.1016/j.jconrel.2005.01.001.

    CAS  Article  PubMed  Google Scholar 

  73. 73.

    Kean T, Thanou M. Biodegradation, biodistribution and toxicity of chitosan. Adv Drug Deliv Rev. 2010;62(1):3–11. https://doi.org/10.1016/j.addr.2009.09.004.

    CAS  Article  PubMed  Google Scholar 

  74. 74.

    Lim SM, Song DK, Oh SH, Lee-Yoon DS, Bae EH, Lee JH. In vitro and in vivo degradation behavior of acetylated chitosan porous beads. J Biomater Sci Polym Ed. 2008;19(4):453–66. https://doi.org/10.1163/156856208783719482.

    CAS  Article  PubMed  Google Scholar 

  75. 75.

    Sashiwa H. Chemical aspects of chitin and chitosan derivatives. In: Kim SK, editor. Chitin and chitosan derivatives: advances in drug discovery and developments. Boca Raton: CRC, Taylor &Francis Group; 2014. p. 93–111.

    Google Scholar 

  76. 76.

    Mourya VK, Inamdar NN, Choudhari YM. Chitooligosaccharides: synthesis, characterization and applications. Polym Sci. 2011;53(7):583–612. https://doi.org/10.1134/s0965545x11070066.

    CAS  Article  Google Scholar 

  77. 77.

    Lodhi G, Kim Y-S, Hwang J-W, Kim S-K, Jeon Y-J, Je J-Y, et al. Chitooligosaccharide and its derivatives: preparation and biological applications. Biomed Res Int. 2014;2014:654913. https://doi.org/10.1155/2014/654913.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Ruiz GAM, Corrales HFZ. Chitosan, chitosan derivatives and their biomedical applications. In: Shalaby EA (Ed)r: Biological Activities and Application of Marine Polysaccharides. Rijeka, Croatia: InTech; 2017. pp: 87-106. https://doi.org/10.5772/66527.

  79. 79.

    Zhao D, Yu S, Sun B, Gao S, Guo S, Zhao K. Biomedical applications of chitosan and its derivative nanoparticles. Polymers. 2018;10(4):462. https://doi.org/10.3390/polym10040462.

    CAS  Article  PubMed Central  Google Scholar 

  80. 80.

    Sayın B, Şenel S. Chitosan and its derivatives for mucosal immunization. In: Jayakumar R, Prabaharan M, editors. Current research and developments on chitin and chitosan in biomaterials science; 2008. p. 145–65.

    Google Scholar 

  81. 81.

    Sayın B, Somavarapu S, Li XW, Thanou M, Sesardic D, Alpar HO, et al. Mono-N-carboxymethyl chitosan (MCC) and N-trimethyl chitosan (TMC) nanoparticles for non-invasive vaccine delivery. Int J Pharm. 2008;363(1–2):139–48. https://doi.org/10.1016/j.ijpharm.2008.06.029.

    CAS  Article  PubMed  Google Scholar 

  82. 82.

    Sayın B, Somavarapu S, Li XW, Sesardic D, Şenel S, Alpar OH. TMC-MCC (N-trimethyl chitosan-mono-N-carboxymethyl chitosan) nanocomplexes for mucosal delivery of vaccines. Eur J Pharm Sci. 2009;38(4):362–9. https://doi.org/10.1016/j.ejps.2009.08.010.

    CAS  Article  PubMed  Google Scholar 

  83. 83.

    Wang W, Meng Q, Li Q, Liu J, Zhou M, Jin Z, et al. Chitosan derivatives and their application in biomedicine. Int J Mol Sci. 2020;21(2):487. https://doi.org/10.3390/ijms21020487.

    CAS  Article  PubMed Central  Google Scholar 

  84. 84.

    Liu H, Wang C, Li C, Qin Y, Wang Z, Yang F, et al. A functional chitosan-based hydrogel as a wound dressing and drug delivery system in the treatment of wound healing. RSC Adv. 2018;8(14):7533–49. https://doi.org/10.1039/c7ra13510f.

    CAS  Article  Google Scholar 

  85. 85.

    Naseri M, Akbarzadeh A, Spotin A, Akbari NAR, Mahami-Oskouei M, Ahmadpour E. Scolicidal and apoptotic activities of albendazole sulfoxide and albendazole sulfoxide-loaded PLGA-PEG as a novel nanopolymeric particle against Echinococcus granulosus protoscoleces. Parasitol Res. 2016;115:4595–603. https://doi.org/10.1007/s00436-016-5250-8.

    Article  PubMed  Google Scholar 

  86. 86.

    Dai T, Tanaka M, Huang Y-Y, Hamblin MR. Chitosan preparations for wounds and burns: antimicrobial and wound-healing effects. Expert Rev Anti-Infect Ther. 2011;9(7):857–79. https://doi.org/10.1586/eri.11.59.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Şenel S, McClure SJ. Potential applications of chitosan in veterinary medicine. Adv Drug Deliv Rev. 2004;56(10):1467–80. https://doi.org/10.1016/j.addr.2004.02.007.

    CAS  Article  PubMed  Google Scholar 

  88. 88.

    Şenel S. Potential applications of chitosan in oral mucosal delivery. J Drug Del Sci Tech. 2010;20(1):23–32. https://doi.org/10.1016/S1773-2247(10)50003-0.

    Article  Google Scholar 

  89. 89.

    Kim J, Cai Z, Lee HS, Choi GS, Lee DH, Jo C. Preparation and characterization of a bacterial cellulose/chitosan composite for potential biomedical application. J Polym Res. 2011;18:739–44. https://doi.org/10.1007/s10965-010-9470-9.

    CAS  Article  Google Scholar 

  90. 90.

    Akca G, Özdemir A, Öner ZG, Şenel S. Comparison of different types and sources of chitosan for the treatment of infections in the oral cavity. Res Chem Intermed. 2018;44:4811–25. https://doi.org/10.1007/s11164-018-3338-8.

    CAS  Article  Google Scholar 

  91. 91.

    Akıncıbay H, Şenel S, Ay ZY. Application of chitosan gel in the treatment of chronic periodontitis. J Biomed Mater Res B Appl Biomater. 2007;80(2):290–6. https://doi.org/10.1002/jbm.b.30596.

    CAS  Article  Google Scholar 

  92. 92.

    Boynueğri D, Özcan G, Şenel S, Uç D, Uraz A, Ögüs E, et al. Clinical and radiographic evaluations of chitosan gel in periodontal intraosseous defects: a pilot study. J Biomed Mater Res B Appl Biomater. 2009;90B:461–6. https://doi.org/10.1002/jbm.b.31307.

    CAS  Article  Google Scholar 

  93. 93.

    Martin L, Wilson CG, Koosha F, Tetley L, Gray AI, Şenel S, et al. The release of model macromolecules may be controlled by the hydrophobicity of palmitoyl glycol chitosan hydrogels. J Control Release. 2002;80(1–3):87–100. https://doi.org/10.1016/s0168-3659(02)00005-6.

    CAS  Article  PubMed  Google Scholar 

  94. 94.

    Özmeriç N, Özcan G, Haytaç CM, Alaaddinoğlu EE, Sargon MF, Şenel S. Chitosan film enriched with an antioxidant agent, taurine, in fenestration defects. J Biomed Mater Res. 2000;51(3):500–3. https://doi.org/10.1002/1097-4636(20000905)51:3<500::AID-JBM26>3.0.CO;2-P.

    Article  PubMed  Google Scholar 

  95. 95.

    Zubareva A, Ily'Ina A, Prokhorov A, Kurek D, Efremov M, Varlamov V, et al. Characterization of protein and peptide binding to nanogels formed by differently charged chitosan derivatives. Molecules. 2013;18(7):7848–64. https://doi.org/10.3390/molecules18077848.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  96. 96.

    Azeran NSB, Zazali NDB, Timur SS, Özdogan AI, Ekizoglu M, Sheshala R, et al. Moxifloxacin loaded chitosan gel formulations for the treatment of periodontal diseases. J Polym Mater. 2017;34(1):157–69.

    Google Scholar 

  97. 97.

    Şenel S, İkinci G, Kaş S, Yousefi-Rad A, Sargon MF, Hıncal AA. Chitosan films and hydrogels of chlorhexidine gluconate for oral mucosal delivery. Int J Pharm. 2000;193(2):197–203. https://doi.org/10.1016/s0378-5173(99)00334-8.

    Article  PubMed  Google Scholar 

  98. 98.

    Sandri G, Rossi S, Ferrari F, Bonferoni MC, Muzzarelli C, Caramella C. Assessment of chitosan derivatives as buccal and vaginal penetration enhancers. Eur J Pharm Sci. 2004;21(2–3):351–9. https://doi.org/10.1016/j.ejps.2003.10.028.

    CAS  Article  PubMed  Google Scholar 

  99. 99.

    Netsomboon K, Bernkop-Schnürch A. Mucoadhesive vs. mucopenetrating particulate drug delivery. Eur J Pharm Biopharm. 2016;98:76–89. https://doi.org/10.1016/j.ejpb.2015.11.003.

    CAS  Article  PubMed  Google Scholar 

  100. 100.

    Şenel S, Kremer MJ, Kaş S, Wertz PW, Hıncal AA, Squier CA. Enhancing effect of chitosan on peptide drug delivery across buccal mucosa. Biomaterials. 2000;21(20):2067–71. https://doi.org/10.1016/s0142-9612(00)00134-4.

    Article  PubMed  Google Scholar 

  101. 101.

    Tokumitsu H, Ichikawa H, Fukumori Y. Chitosan-gadopentetic acid complex nanoparticles for gadolinium neutron-capture therapy of cancer: preparation by novel emulsion-droplet coalescence technique and characterization. Pharm Res. 1999;16:1830–5. https://doi.org/10.1023/a:1018995124527.

    CAS  Article  PubMed  Google Scholar 

  102. 102.

    Calvo P, Remunan-Lopez C, Vila-Jato JL, Alonso MJ. Novel hydrophilic chitosan-polyethylene oxide nanoparticles as protein carriers. J Appl Polym Sci. 1997;63(1):125–32. https://doi.org/10.1002/(SICI)1097-4628(19970103)63:1<125::AID-APP13>3.0.CO;2-4.

    CAS  Article  Google Scholar 

  103. 103.

    Sarmento B, Martins S, Ribeiro A, Veiga F, Neufeld R, Ferreira D. Development and comparison of different nanoparticulate polyelectrolyte complexes as insulin carriers. Int J Pept Res Ther. 2006;12(2):131–8. https://doi.org/10.1007/s10989-005-9010-3.

    CAS  Article  Google Scholar 

  104. 104.

    El-Shabouri MH. Positively charged nanoparticles for improving the oral bioavailability of cyclosporin-A. Int J Pharm. 2002;249(1–2):101–8. https://doi.org/10.1016/s0378-5173(02)00461-1.

    CAS  Article  PubMed  Google Scholar 

  105. 105.

    Mitra S, Gaur U, Ghosh PC, Maitra AN. Tumour targeted delivery of encapsulated dextran-doxorubicin conjugate using chitosan nanoparticles as carrier. J Control Release. 2001;74(1–3):317–23. https://doi.org/10.1016/s0168-3659(01)00342-x.

    CAS  Article  PubMed  Google Scholar 

  106. 106.

    Tian XX, Groves MJ. Formulation and biological activity of antineoplastic proteoglycans derived from Mycobacterium vaccae in chitosan nanoparticles. J Pharm Pharmacol. 1999;51(2):151–7. https://doi.org/10.1211/0022357991772268.

    CAS  Article  PubMed  Google Scholar 

  107. 107.

    Ohya Y, Shiratani M, Kobayashi H, Ouchi T. Release behavior of 5-fluorouracil from chitosan-gel nanospheres immobilizing 5-fluorouracil coated with polysaccharides and their cell specific cytotoxicity. J Macromol Sci A. 1994;31(5):629–42. https://doi.org/10.1080/10601329409349743.

    Article  Google Scholar 

  108. 108.

    Grenha A. Chitosan nanoparticles: a survey of preparation methods. J Drug Target. 2012;20(4):291–300. https://doi.org/10.3109/1061186x.2011.654121.

    CAS  Article  PubMed  Google Scholar 

  109. 109.

    Liu C, Tan Y, Liu C, Chen X, Yu L. Preparations, characterizations and applications of chitosan-based nanoparticles. J Ocean U China. 2007;6(3):237–43. https://doi.org/10.1007/s11802-007-0237-9.

    CAS  Article  Google Scholar 

  110. 110.

    Lee JW, Park JH, Robinson JR. Bioadhesive-based dosage forms: the next generation. J Pharm Sci. 2000;89(7):850–66. https://doi.org/10.1002/1520-6017(200007)89:7.

    CAS  Article  PubMed  Google Scholar 

  111. 111.

    Peppas N, Huang Y. Nanoscale technology of mucoadhesive interaction. Adv Drug Deliv Rev. 2004;56:1675–87. https://doi.org/10.1016/j.addr.2004.03.001.

    CAS  Article  PubMed  Google Scholar 

  112. 112.

    Luessen HL, de Leeuw BJ, Langemeyer MW, de Boer AB, Verhoef JC, Junginger HE. Mucoadhesive polymers in peroral peptide drug delivery. VI. Carbomer and chitosan improve the intestinal absorption of the peptide drug buserelin in vivo. Pharm Res. 1996;13(11):1668–72. https://doi.org/10.1023/a:1016488623022.

    CAS  Article  PubMed  Google Scholar 

  113. 113.

    Furda I. Reduction of absorption of dietary lipids and cholesterol by chitosan and its derivatives and special formulations. In: Muzzareilli RAA, editor. Chitosan per os: from dietary supplement to drug carrier. Grottammare: Atec; 2000. p. 41–63.

    Google Scholar 

  114. 114.

    Thanou M, Verhoef JC, Junginger HE. Oral drug absorption enhancement by chitosan and its derivatives. Adv Drug Deliv Rev. 2001;52(2):117–26. https://doi.org/10.1016/s0169-409x(01)00231-9.

    CAS  Article  PubMed  Google Scholar 

  115. 115.

    Sonia TA, Sharma CP. Chitosan and its derivatives for drug delivery perspective. In: Jayakumar R, Prabaharan M, Muzzarelli RAA, editors. Chitosan for biomaterials I. Berlin: Springer; 2011. p. 23–53.

    Google Scholar 

  116. 116.

    Bernkop-Schnürch A, Dünnhaupt S. Chitosan-based drug delivery systems. Eur J Pharm Sci. 2012;81(3):463–9. https://doi.org/10.1016/j.ejpb.2012.04.007.

    CAS  Article  Google Scholar 

  117. 117.

    Singh PK, Pawar VK, Jaiswal AK, Singh Y, Srikanth CH, Chaurasia M, et al. Chitosan coated PluronicF127 micelles for effective delivery of amphotericin B in experimental visceral leishmaniasis. Int J Biol Macromol. 2017;105(1):1220–31. https://doi.org/10.1016/j.ijbiomac.2017.07.161.

    CAS  Article  PubMed  Google Scholar 

  118. 118.

    Jain V, Gupta A, Pawar VK, Asthana S, Jaiswal AK, Dube A, et al. Chitosan-assisted immunotherapy for intervention of experimental leishmaniasis via amphotericin B-loaded solid lipid nanoparticles. Appl Biochem Biotechnol. 2014;174:1309–30. https://doi.org/10.1007/s12010-014-1084-y.

    CAS  Article  PubMed  Google Scholar 

  119. 119.

    Gupta PK, Asthana S, Jaiswal AK, Kumar V, Verma AK, Shukla P, et al. Exploitation of lectinized lipo-polymerosome encapsulated amphotericin B to target macrophages for effective chemotherapy of visceral leishmaniasis. Bioconjug Chem. 2014;25(6):1091–102. https://doi.org/10.1021/bc500087h.

    CAS  Article  PubMed  Google Scholar 

  120. 120.

    Vemireddy S, Preethi Pallavi MC, Sampath Kumar Halmuthur M. Chitosan stabilized nasal emulsion delivery system for effective humoral and cellular response against recombinant tetravalent dengue antigen. Carbohydr Polym. 2018;190:129–38. https://doi.org/10.1016/j.carbpol.2018.02.073.

    CAS  Article  PubMed  Google Scholar 

  121. 121.

    Neimert-Andersson T, Binnmyr J, Enoksson M, Langeback J, Zettergren L, Hallgren AC, et al. Evaluation of safety and efficacy as an adjuvant for the chitosan-based vaccine delivery vehicle ViscoGel in a single-blind randomised phase I/IIa clinical trial. Vaccine. 2014;32(45):5967–74. https://doi.org/10.1016/j.vaccine.2014.08.057.

    CAS  Article  PubMed  Google Scholar 

  122. 122.

    Arca HC, Günbeyaz M, Şenel S. Chitosan-based systems for the delivery of vaccine antigens. Expert Rev Vaccines. 2009;8(7):937–53. https://doi.org/10.1586/erv.09.47.

    CAS  Article  PubMed  Google Scholar 

  123. 123.

    Şenel S. Chitosan-based particulate systems for non-invasive vaccine delivery. In: Jayakumar R, Prabaharan M, RAA M, editors. Advances in polymer sciences. Berlin: Springer; 2011. p. 111–37.

    Google Scholar 

  124. 124.

    Çokçalışkan C, Özyörük F, Gürsoy RN, Alkan M, Günbeyaz M, Arca HÇ, et al. Chitosan-based systems for intranasal immunization against foot-and-mouth disease. Pharm Dev Technol. 2014;19(2):181–8. https://doi.org/10.3109/10837450.2013.763263.

    CAS  Article  PubMed  Google Scholar 

  125. 125.

    Huo Z, Sinha R, McNeela EA, Borrow R, Giemza R, Cosgrove C, et al. Induction of protective serum meningococcal bactericidal and diphtheria-neutralizing antibodies and mucosal immunoglobulin a in volunteers by nasal insufflations of the Neisseria meningitidis serogroup C polysaccharide-CRM197 conjugate vaccine mixed with chitosan. Infect Immun. 2005;73(12):8256–65. https://doi.org/10.1128/IAI.73.12.8256-8265.2005.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  126. 126.

    Zaharoff DA, Rogers CJ, Hance KW, Schlom J, Greiner JW. Chitosan solution enhances both humoral and cell-mediated immune responses to subcutaneous vaccination. Vaccine. 2007;25(11):2085–94. https://doi.org/10.1016/j.vaccine.2006.11.034.

    CAS  Article  PubMed  Google Scholar 

  127. 127.

    McNeela EA, Jabbal-Gill I, Illum L, Pizza M, Rappuoli R, Podda A, et al. Intranasal immunization with genetically detoxified diphtheria toxin induces T cell responses in humans: enhancement of Th2 responses and toxin-neutralizing antibodies by formulation with chitosan. Vaccine. 2004;22(8):909–14. https://doi.org/10.1016/j.vaccine.2003.09.012.

    CAS  Article  PubMed  Google Scholar 

  128. 128.

    Read RC, Naylor SC, Potter CW, Bond J, Jabbal-Gill I, Fisher A, et al. Effective nasal influenza vaccine delivery using chitosan. Vaccine. 2005;23(35):4367–74. https://doi.org/10.1016/j.vaccine.2005.04.021.

    CAS  Article  PubMed  Google Scholar 

  129. 129.

    Atmar RL, Bernstein DI, Harro CD, Al-Ibrahim MS, Chen WH, Ferreira J, et al. Norovirus vaccine against experimental human Norwalk virus illness. N Engl J Med. 2011;365(23):2178–87. https://doi.org/10.1056/nejmoa1101245.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  130. 130.

    Yüksel S, Pekcan M, Puralı N, Esendağlı G, Tavukçuoğlu E, Rivero-Arredondo V, et al. Development and in vitro evaluation of a new adjuvant system containing Salmonella Typhi porins and chitosan. Int J Pharm. 2020;578:119129. https://doi.org/10.1016/j.ijpharm.2020.119129.

    CAS  Article  PubMed  Google Scholar 

  131. 131.

    Peluso G, Petillo O, Ranieri M, Santin M, Ambrosio L, Calabro D, et al. Chitosan-mediated stimulation of macrophage function. Biomaterials. 1994;15(15):1215–20. https://doi.org/10.1016/0142-9612(94)90272-0.

    CAS  Article  PubMed  Google Scholar 

  132. 132.

    Nishimura K, Nishimura S, Nishi N, Saiki I, Tokura S, Azuma I. Immunological activity of chitin and its derivatives. Vaccine. 1984;2(1):93–9. https://doi.org/10.1016/s0264-410x(98)90039-1.

    CAS  Article  PubMed  Google Scholar 

  133. 133.

    Carroll EC, Jin L, Mori A, Munoz-Wolf N, Oleszycka E, Moran HBT, et al. The vaccine adjuvant chitosan promotes cellular immunity via DNA sensor cGAS-STING-dependent induction of type I interferons. Immunity. 2016;44(3):597–608. https://doi.org/10.1016/j.immuni.2016.02.004.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  134. 134.

    Scherließ R, Buske S, Young K, Weber B, Rades T, Hook S. In vivo evaluation of chitosan as an adjuvant in subcutaneous vaccine formulations. Vaccine. 2013;31(42):4812–9. https://doi.org/10.1016/j.vaccine.2013.07.081.

    CAS  Article  PubMed  Google Scholar 

  135. 135.

    Moran HBT, Turley JL, Andersson M, Lavelle EC. Immunomodulatory properties of chitosan polymers. Biomaterials. 2018;184:1–9. https://doi.org/10.1016/j.biomaterials.2018.08.054.

    CAS  Article  PubMed  Google Scholar 

  136. 136.

    Ravindranathan S, Koppolu B, Smith S, Zaharoff D. Effect of chitosan properties on immunoreactivity. Mar Drugs. 2016;14(5):91. https://doi.org/10.3390/md14050091.

    CAS  Article  PubMed Central  Google Scholar 

  137. 137.

    Ragelle H, Vandermeulen G, Préat V. Chitosan-based siRNA delivery systems. J Control Release. 2013;172(1):207–18. https://doi.org/10.1016/j.jconrel.2013.08.005.

    CAS  Article  PubMed  Google Scholar 

  138. 138.

    Şenel S, Aksoy EA, Akca G. Application of chitosan based scaffolds for drug delivery and tissue engineering in dentistry. In: Choi A, Ben-Nissan B, editors. Marine-derived biomaterials for tissue engineering applications. Springer Series in biomaterials science and engineering, vol. 14. Singapore: Springer; 2019. p. 157–78. https://doi.org/10.1007/978-981-13-8855-2_8.

    Google Scholar 

  139. 139.

    Li P, Poon YF, Li W, Zhu H-Y, Yeap SH, Cao Y, et al. A polycationic antimicrobial and biocompatible hydrogel with microbe membrane suctioning ability. Nat Mater. 2011;10:149–56. https://doi.org/10.1038/nmat2915.

    CAS  Article  PubMed  Google Scholar 

  140. 140.

    Andres Y, Giraud L, Gerente C, Le Cloirec P. Antibacterial effects of chitosan powder: mechanisms of action. Environ Technol. 2007;28(12):1357–63. https://doi.org/10.1080/09593332808618893.

    CAS  Article  PubMed  Google Scholar 

  141. 141.

    Raafat D, Von Bargen K, Haas A, Sahl HG. Insights into the mode of action of chitosan as an antibacterial compound. Appl Environ Microbiol. 2008;74(12):3764–73. https://doi.org/10.1128/aem.00453-08.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  142. 142.

    Rabea EI, Badawy ME, Stevens CV, Smagghe G, Steurbaut W. Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules. 2003;4(6):1457–65. https://doi.org/10.1021/bm034130m.

    CAS  Article  PubMed  Google Scholar 

  143. 143.

    Kong M, Chen XG, Xing K, Park HJ. Antimicrobial properties of chitosan and mode of action: a state of the art review. Int J Food Microbiol. 2010;144(1):51–63. https://doi.org/10.1016/j.ijfoodmicro.2010.09.012.

    CAS  Article  PubMed  Google Scholar 

  144. 144.

    Prudden JF, Migel P, Hanson P, Friedrich L, Balassa L. The discovery of a potent pure chemical wound-healing accelerator. Am J Surg. 1970;119(5):560–4. https://doi.org/10.1016/0002-9610(70)90175-3.

    CAS  Article  PubMed  Google Scholar 

  145. 145.

    Muzzarelli RA, Mattioli-Belmonte M, Pugnaloni A, Biagini G. Biochemistry, histology and clinical uses of chitins and chitosans in wound healing. In: Jolles P, Muzzarelli RA, editors. Chitin and chitinases. 1st ed. Basel: Birkhäuser; 1999. p. 251–64.

    Google Scholar 

  146. 146.

    Ueno H, Nakamura F, Murakami M, Okumura M, Kadosawa T, Fujinaga T. Evaluation effects of chitosan for the extracellular matrix production by fibroblasts and the growth factors production by macrophages. Biomaterials. 2001;22(15):2125–30. https://doi.org/10.1016/s0142-9612(00)00401-4.

    CAS  Article  PubMed  Google Scholar 

  147. 147.

    Suzuki Y. Influence of physico-chemical properties of chitin and chitosan on complement activation. Carbohydr Polym. 2000;42(3):307–10. https://doi.org/10.1016/s0144-8617(99)00161-7.

    CAS  Article  Google Scholar 

  148. 148.

    Ueno H, Mori T, Fujinaga T. Topical formulations and wound healing applications of chitosan. Adv Drug Deliv Rev. 2001;52(2):105–15. https://doi.org/10.1016/s0169-409x(01)00189-2.

    CAS  Article  PubMed  Google Scholar 

  149. 149.

    Hu Z, Zhang D-Y, Lu S-T, Li P-W, Li S-D. Chitosan-based composite materials for prospective hemostatic applications. Mar Drugs. 2018;16(8). https://doi.org/10.3390/md16080273.

  150. 150.

    WHO. Dengue and severe dengue. https://www.who.int/news-room/fact-sheets/detail/dengue-and-severe-dengue; (accessed 24 March 2020).

  151. 151.

    Sanofi. Dengue. https://www.sanofi.com/en/your-health/vaccines/dengue; (accessed 24 March 2020).

  152. 152.

    Hunsawong T, Sunintaboon P, Warit S, Thaisomboonsuk B, Jarman RG, Yoon I-K, et al. Immunogenic properties of a BCG adjuvanted chitosan nanoparticle-based dengue vaccine in human dendritic cells. PLoS Negl Trop Dis. 2015;9(9):e0003958. https://doi.org/10.1371/journal.pntd.0003958.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  153. 153.

    Hunsawong T, Sunintaboon P, Warit S, Thaisomboonsuk B, Jarman RG, Yoon I-K, et al. A novel dengue virus serotype-2 nanovaccine induces robust humoral and cell-mediated immunity in mice. Vaccine. 2015;33(14):1702–10. https://doi.org/10.1016/j.vaccine.2015.02.016.

    CAS  Article  PubMed  Google Scholar 

  154. 154.

    Nantachit N, Sunintaboon P, Ubol S. EDIII-DENV3 nanospheres drive immature dendritic cells into a mature phenotype in an in vitro model. Microbiol Immunol. 2017;61:305–17. https://doi.org/10.1111/1348-0421.12497.

    CAS  Article  PubMed  Google Scholar 

  155. 155.

    Nantachit N, Sunintaboon P, Ubol S. Responses of primary human nasal epithelial cells to EDIII-DENV stimulation: the first step to intranasal dengue vaccination. Virol J. 2016;13:142. https://doi.org/10.1186/s12985-016-0598-z.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  156. 156.

    Izaguirre-Hernandez IY, Mellado-Sanchez G, Mondragon-Vasquez K, Thomas-Dupont P, Sanchez-Vargas LA, Hernandez-Flores KG, et al. Non-conjugated chitosan-based nanoparticles to proteic antigens elicit similar humoral immune responses to those obtained with alum. J Nanosci Nanotechnol. 2017;17(1):846–52. https://doi.org/10.1166/jnn.2017.13067.

    CAS  Article  PubMed  Google Scholar 

  157. 157.

    Cavalcanti IT, Silva BVM, Peres NG, Moura P, Sotomayor MDPT, Guedes MIF, et al. A disposable chitosan-modified carbon fiber electrode for dengue virus envelope protein detection. Talanta. 2012;91:41–6. https://doi.org/10.1016/j.talanta.2012.01.002.

    CAS  Article  PubMed  Google Scholar 

  158. 158.

    Leonardi D, Salomón CJ, Lamas MC, Olivieri AC. Development of novel formulations for Chagas’ disease: optimization of benznidazole chitosan microparticles based on artificial neural networks. Int J Pharm. 2009;367(1–2):140–7. https://doi.org/10.1016/j.ijpharm.2008.09.036.

    CAS  Article  PubMed  Google Scholar 

  159. 159.

    Nhavene EPF, Da Silva WM, Trivelato Junior RR, Gastelois PL, Venâncio T, Nascimento R, et al. Chitosan grafted into mesoporous silica nanoparticles as benznidazol carrier for Chagas diseases treatment. Microporous Mesoporous Mater. 2018;272:265–75. https://doi.org/10.1016/j.micromeso.2018.06.035.

    CAS  Article  Google Scholar 

  160. 160.

    Vespa GN, Cunha FQ, Silva JS. Nitric oxide is involved in control of Trypanosoma cruzi-induced parasitemia and directly kills the parasite in vitro. Infect Immun. 1994;62(11):5177–82.

    CAS  Article  Google Scholar 

  161. 161.

    Seabra AB, Durán N. Chapter 2 - nitric oxide donors for treating neglected diseases. In: Seabra AB, editor. Nitric oxide donors. London: Academic; 2017. p. 25–53.

    Google Scholar 

  162. 162.

    Gutierrez FR, Mineo TW, Pavanelli WR, Guedes PM, Silva JS. The effects of nitric oxide on the immune system during Trypanosoma cruzi infection. Mem Inst Oswaldo Cruz. 2009;104:236–45. https://doi.org/10.1590/s0074-02762009000900030.

    CAS  Article  PubMed  Google Scholar 

  163. 163.

    Seabra AB, Kitice NA, Pelegrino MT, Lancheros CAC, Yamauchi LM, Pinge-Filho P, et al. Nitric oxide-releasing polymeric nanoparticles against Trypanosoma cruzi. J Phys Conf Ser. 2015;617:012020. https://doi.org/10.1088/1742-6596/617/1/012020.

    CAS  Article  Google Scholar 

  164. 164.

    Contreras Lancheros CA, Pelegrino MT, Kian D, Tavares ER, Hiraiwa PM, Goldenberg S, et al. Selective antiprotozoal activity of nitric oxide-releasing chitosan nanoparticles against Trypanosoma cruzi: toxicity and mechanisms of action. Curr Pharm Des. 2018;24(7):830–9. https://doi.org/10.2174/1381612824666180209105625.

    CAS  Article  PubMed  Google Scholar 

  165. 165.

    WHO. Echinococcosis. https://www.who.int/news-room/fact-sheets/detail/echinococcosis; (accessed 02 December 2019).

  166. 166.

    Torabi N, Dobakhti F, Faghihzadeh S, Haniloo A. In vitro and in vivo effects of chitosan-praziquantel and chitosan-albendazole nanoparticles on Echinococcus granulosus Metacestodes. Parasitol Res. 2018;117:2015–23. https://doi.org/10.1007/s00436-018-5849-z.

    Article  PubMed  Google Scholar 

  167. 167.

    Liu Y, Wang X-Q, Ren W-X, Chen Y-L, Yu Y, Zhang J-K, et al. Novel albendazole-chitosan nanoparticles for intestinal absorption enhancement and hepatic targeting improvement in rats. J Biomed Mater Res B Appl Biomater. 2013;101B(6):998–1005. https://doi.org/10.1002/jbm.b.32908.

    CAS  Article  Google Scholar 

  168. 168.

    Abulaihaiti M, Wu X-W, Qiao L, Lv H-L, Zhang H-W, Aduwayi N, et al. Efficacy of albendazole-chitosan microsphere-based treatment for alveolar echinococcosis in mice. PLoS Negl Trop Dis. 2015;9(9):e0003950. https://doi.org/10.1371/journal.pntd.0003950.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  169. 169.

    Araújo C, Leon L. Biological activities of Curcuma longa L. Mem Inst Oswaldo Cruz. 2001;96(5):723–8. https://doi.org/10.1590/s0074-02762001000500026.

    Article  PubMed  Google Scholar 

  170. 170.

    Napooni S, Delavari M, Arbabi M, Barkheh H, Rasti S, Hooshyar H, et al. Scolicidal effects of chitosan-curcumin nanoparticles on the hydatid cyst protoscolices. Acta Parasitol. 2019;64:367–75. https://doi.org/10.2478/s11686-019-00054-8.

    Article  PubMed  Google Scholar 

  171. 171.

    WHO. Leishmaniasis. https://www.who.int/news-room/fact-sheets/detail/leishmaniasis; (accessed 10 March 2020).

  172. 172.

    Bahrami S, Esmaeilzadeh S, Zarei M, Ahmadi F. Potential application of nanochitosan film as a therapeutic agent against cutaneous leishmaniasis caused by L. major. Parasitol Res. 2015;114(12):4617–24. https://doi.org/10.1007/s00436-015-4707-5.

    Article  PubMed  Google Scholar 

  173. 173.

    Riezk A, Raynes JG, Yardley V, Murdan S, Croft SL. Activity of chitosan and its derivatives against Leishmania major and L. mexicana in vitro. Antimicrob Agents Chemother. 2019;64:e01772–19. https://doi.org/10.1128/aac.01772-19.

    CAS  Article  Google Scholar 

  174. 174.

    Esboei B, Mohebali M, Mousavi P, Fakhar M, Akhoundi B. Potent antileishmanial activity of chitosan against Iranian strain of Leishmania major (MRHO/IR/75/ER): in vitro and in vivo assay. J Vector Borne Dis. 2018;55:111–5. https://doi.org/10.4103/0972-9062.242557.

    CAS  Article  PubMed  Google Scholar 

  175. 175.

    Abdollahimajd FMH, Dadkhahfar S, Mahdavi H, Mohebali M, Mirzadeh H. Chitosan-based biocompatible dressing for treatment of recalcitrant lesions of cutaneous leishmaniasis: a pilot clinical study. Indian J Dermatol Venereol Leprol. 2019;85:609–14. https://doi.org/10.4103/ijdvl.IJDVL_189_18.

    Article  PubMed  Google Scholar 

  176. 176.

    Danesh-Bahreini MASJ, Samiei A, Kamali-Sarvestani E, Barzegar-Jalali M, Mohammadi-Samani S. Nanovaccine for leishmaniasis: preparation of chitosan nanoparticles containing Leishmania superoxide dismutase and evaluation of its immunogenicity in BALB/c mice. Int J Nanomedicine. 2011;6:835–42. https://doi.org/10.2147/ijn.s16805.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  177. 177.

    Yeganeh F, Barkhordari F, Omidi M, Samiei A, Adeli A, Mahboudi F, et al. Cloning and expression of Leishmania major superoxide dismutase B1: a potential target antigen for serodiagnosis of Leishmaniasis. Iran J Immunol. 2009;6(3):130–40.

    CAS  PubMed  Google Scholar 

  178. 178.

    Hojatizade M, Soleymani M, Tafaghodi M, Badiee A, Chavoshian O, Jaafari MR. Chitosan nanoparticles loaded with whole and soluble Leishmania antigens, and evaluation of their immunogenecity in a mouse model of leishmaniasis. Iran J Immunol. 2018;15(4):281–93. https://doi.org/10.22034/IJI.2018.39397.

    Article  PubMed  Google Scholar 

  179. 179.

    Esfandiari F, Motazedian MH, Asgari Q, Morowvat MH, Molaei M, Heli H. Paromomycin-loaded mannosylated chitosan nanoparticles: synthesis, characterization and targeted drug delivery against leishmaniasis. Acta Trop. 2019;197:105045. https://doi.org/10.1016/j.actatropica.2019.105045.

    CAS  Article  PubMed  Google Scholar 

  180. 180.

    Chaubey P, Mishra B. Mannose-conjugated chitosan nanoparticles loaded with rifampicin for the treatment of visceral leishmaniasis. Carbohydr Polym. 2014;101:1101–8. https://doi.org/10.1016/j.carbpol.2013.10.044.

    CAS  Article  PubMed  Google Scholar 

  181. 181.

    Monteiro LM, Lobenberg R, Fotaki N, de Araujo GLB, Cotrim PC, Bou-Chacra N. Co-delivery of buparvaquone and polymyxin B in a nanostructured lipid carrier for leishmaniasis treatment. J Glob Antimicrob Resist. 2019;18:279–83. https://doi.org/10.1016/j.jgar.2019.06.006.

    Article  PubMed  Google Scholar 

  182. 182.

    Yamamoto ES, Campos BLS, Jesus JA, Laurenti MD, Ribeiro SP, Kallás EG, et al. The effect of ursolic acid on Leishmania (Leishmania) amazonensis is related to programed cell death and presents therapeutic potential in experimental cutaneous leishmaniasis. PLoS One. 2015;10(12):e0144946. https://doi.org/10.1371/journal.pone.0144946.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  183. 183.

    Santos-Valle ABC, Souza GRR, Paes CQ, Miyazaki T, Silva AH, Altube MJ, et al. Nanomedicine strategies for addressing major needs in neglected tropical diseases. Annu Rev Control. 2019;48:423–41. https://doi.org/10.1016/j.arcontrol.2019.08.001.

    Article  Google Scholar 

  184. 184.

    Frézard F, Demicheli C, Da Silva SM, Azevedo EG, Ribeiro RR. ,Nanostructures for improved antimonial therapy of leishmaniasis. In: Grumezescu AM (Ed.) Nano- and Microscale Drug Delivery Systems. Philadelphia, US: Elsevier; 2017. pp. 419–37. https://doi.org/10.1016/B978-0-323-52727-9.00022-4.

  185. 185.

    Tripathi P, Dwivedi P, Khatik R, Jaiswal AK, Dube A, Shukla P, et al. Development of 4-sulfated N-acetyl galactosamine anchored chitosan nanoparticles: a dual strategy for effective management of leishmaniasis. Colloids Surf B. 2015;136:150–9. https://doi.org/10.1016/j.colsurfb.2015.08.037.

    CAS  Article  Google Scholar 

  186. 186.

    Tan JSL, Roberts C, Billa N. Pharmacokinetics and tissue distribution of an orally administered mucoadhesive chitosan-coated amphotericin B-loaded nanostructured lipid carrier (NLC) in rats. J Biomater Sci Polym Ed. 2020;31(2):141–54. https://doi.org/10.1080/09205063.2019.1680926.

    CAS  Article  PubMed  Google Scholar 

  187. 187.

    Gupta PK, Jaiswal AK, Kumar V, Verma A, Dwivedi P, Dube A, et al. Covalent functionalized self-assembled lipo-polymerosome bearing amphotericin B for better management of leishmaniasis and its toxicity evaluation. Mol Pharm. 2014;11(3):951–63. https://doi.org/10.1021/mp400603t.

    CAS  Article  PubMed  Google Scholar 

  188. 188.

    Gupta PK, Jaiswal AK, Asthana S, Verma A, Kumar V, Shukla P, et al. Self assembled ionically sodium alginate cross-linked amphotericin B encapsulated glycol chitosan stearate nanoparticles: applicability in better chemotherapy and non-toxic delivery in visceral leishmaniasis. Pharm Res. 2015;32:1727–40. https://doi.org/10.1007/s11095-014-1571-4.

    CAS  Article  PubMed  Google Scholar 

  189. 189.

    Shahnaz G, Edagwa BJ, McMillan J, Akhtar S, Raza A, Qureshi NA, et al. Development of mannose-anchored thiolated amphotericin B nanocarriers for treatment of visceral leishmaniasis. Nanomedicine. 2017;12(2):99–115. https://doi.org/10.2217/nnm-2016-0325.

    CAS  Article  PubMed  Google Scholar 

  190. 190.

    Asthana S, Jaiswal AK, Gupta PK, Pawar VK, Dube A, Chourasia MK. Immunoadjuvant chemotherapy of visceral leishmaniasis in hamsters using amphotericin B-encapsulated nanoemulsion template-based chitosan nanocapsules. Antimicrob Agents Chemother. 2013;57(4):1714–22. https://doi.org/10.1128/aac.01984-12.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  191. 191.

    Asthana S, Gupta PK, Jaiswal AK, Dube A, Chourasia MK. Overexpressed macrophage mannose receptor targeted nanocapsules-mediated cargo delivery approach for eradication of resident parasite: in vitro and in vivo studies. Pharm Res. 2015;32(8):2663–77. https://doi.org/10.1007/s11095-015-1651-0.

    CAS  Article  PubMed  Google Scholar 

  192. 192.

    Ribeiro TG, Chávez-Fumagalli MA, Valadares DG, França JR, Rodrigues LB, Duarte MC, et al. Novel targeting using nanoparticles: an approach to the development of an effective anti-leishmanial drug-delivery system. Int J Nanomedicine. 2014;9:877–90. https://doi.org/10.2147/IJN.S55678.

    Article  PubMed  PubMed Central  Google Scholar 

  193. 193.

    Ribeiro T, Franca J, Fuscaldi L, Santos M, Duarte M, Lage P, et al. An optimized nanoparticle delivery system based on chitosan and chondroitin sulfate molecules reduces the toxicity of amphotericin B and is effective in treating tegumentary leishmaniasis. Int J Nanomedicine. 2014;9:5341–53. https://doi.org/10.2147/ijn.s68966.

    Article  PubMed  PubMed Central  Google Scholar 

  194. 194.

    Bose PP, Kumar P, Dwivedi MK. Hemoglobin guided nanocarrier for specific delivery of amphotericin B to Leishmania infected macrophage. Acta Trop. 2016;158:148–59. https://doi.org/10.1016/j.actatropica.2016.02.026.

    CAS  Article  PubMed  Google Scholar 

  195. 195.

    Serrano DR, Lalatsa A, Dea-Ayuela MA, Bilbao-Ramos PE, Garrett NL, Moger J, et al. Oral particle uptake and organ targeting drives the activity of amphotericin B nanoparticles. Mol Pharm. 2015;12(2):420–31. https://doi.org/10.1021/mp500527x.

    CAS  Article  PubMed  Google Scholar 

  196. 196.

    Cabral FV, Pelegrino MT, Sauter IP, Seabra AB, Cortez M, Ribeiro MS. Nitric oxide-loaded chitosan nanoparticles as an innovative antileishmanial platform. Nitric Oxide. 2019;93:25–33. https://doi.org/10.1016/j.niox.2019.09.007.

    CAS  Article  PubMed  Google Scholar 

  197. 197.

    Rabia S, Khaleeq N, Batool S, Dar MJ, Kim DW, Din FU, et al. Rifampicin-loaded nanotransferosomal gel for treatment of cutaneous leishmaniasis: passive targeting via topical route. Nanomedicine. 2020;15(2):183–203. https://doi.org/10.2217/nnm-2019-0320.

    CAS  Article  PubMed  Google Scholar 

  198. 198.

    Moreno E, Schwartz J, Larrea E, Conde I, Font M, Sanmartín C, et al. Assessment of β-lapachone loaded in lecithin-chitosan nanoparticles for the topical treatment of cutaneous leishmaniasis in L. major infected BALB/c mice. Nanomed-Nanotechnol. 2015;11(8):2003–12. https://doi.org/10.1016/j.nano.2015.07.011.

    CAS  Article  Google Scholar 

  199. 199.

    Malli S, Pomel S, Dennemont I, Loiseau PM, Bouchemal K. Combination of amphotericin B and chitosan platelets for the treatment of experimental cutaneous leishmaniasis: histological and immunohistochemical examinations. J Drug Deliv Sci Tec. 2019;50:34–41. https://doi.org/10.1016/j.jddst.2018.12.031.

    CAS  Article  Google Scholar 

  200. 200.

    Malli S, Pomel S, Ayadi Y, Deloménie C, Da Costa A, Loiseau PM, et al. Topically applied chitosan-coated poly (isobutylcyanoacrylate) nanoparticles are active against cutaneous leishmaniasis by accelerating lesion healing and reducing the parasitic load. ACS Appl Bio Mater. 2019;2(6):2573–86. https://doi.org/10.1021/acsabm.9b00263.

    CAS  Article  Google Scholar 

  201. 201.

    Varshosaz J, Arbabi B, Pestehchian N, Saberi S, Delavari M. Chitosan-titanium dioxide-glucantime nanoassemblies effects on promastigote and amastigote of Leishmania major. Int J Biol Macromol. 2018;107:212–21. https://doi.org/10.1016/j.ijbiomac.2017.08.177.

    CAS  Article  PubMed  Google Scholar 

  202. 202.

    Rafiee A, Riazi-Rad F, Darabi H, Khaze V, Javadian S, Ajdary S, et al. Ferroportin-encapsulated nanoparticles reduce infection and improve immunity in mice infected with Leishmania major. Int J Pharm. 2014;466(1–2):375–81. https://doi.org/10.1016/j.ijpharm.2014.03.039.

    CAS  Article  PubMed  Google Scholar 

  203. 203.

    WHO. Lymphatic filariasis. https://www.who.int/lymphatic_filariasis/disease/en/; (accessed 24 March 2020).

  204. 204.

    Ali M, Afzal M, Verma M, Misra-Bhattacharya S, Ahmad FJ, Dinda AK. Improved antifilarial activity of ivermectin in chitosan–alginate nanoparticles against human lymphatic filarial parasite, Brugia malayi. Parasitol Res. 2013;112(8):2933–43. https://doi.org/10.1007/s00436-013-3466-4.

    Article  PubMed  Google Scholar 

  205. 205.

    Shukla R, Gupta J, Shukla P, Dwivedi P, Tripathi P, Bhattacharya SM, et al. Chitosan coated alginate micro particles for the oral delivery of antifilarial drugs and combinations for intervention in Brugia malayi induced lymphatic filariasis. RSC Adv. 2015;5:69047–56. https://doi.org/10.1039/C5RA06982C.

    CAS  Article  Google Scholar 

  206. 206.

    Madhumathi J, Prince PR, Anugraha G, Kiran P, Rao DN, Reddy MVR, et al. Identification and characterization of nematode specific protective epitopes of Brugia malayi TRX towards development of synthetic vaccine construct for lymphatic filariasis. Vaccine. 2010;28(31):5038–48. https://doi.org/10.1016/j.vaccine.2010.05.012.

    CAS  Article  PubMed  Google Scholar 

  207. 207.

    Gregory WF, Atmadja AK, Allen JE, Maizels RM. The abundant larval transcript-1 and -2 genes of Brugia malayi encode stage-specific candidate vaccine antigens for filariasis. Infect Immun. 2000;68(7):4174–9. https://doi.org/10.1128/iai.68.7.4174-4179.2000.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  208. 208.

    Malathi B, Mona S, Thiyagarajan D, Kaliraj P. Immunopotentiating nano-chitosan as potent vaccine carter for efficacious prophylaxis of filarial antigens. Int J Biol Macromol. 2015;73:131–7. https://doi.org/10.1016/j.ijbiomac.2014.11.014.

    CAS  Article  PubMed  Google Scholar 

  209. 209.

    Oliveira CR, Rezende CMF, Silva MR, Borges OM, Pêgo AP, Goes AM. Oral vaccination based on DNA-chitosan nanoparticles against Schistosoma mansoni infection. ScientificWorldJournal. 2012;2012:938457. https://doi.org/10.1100/2012/938457.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  210. 210.

    Oliveira CR, Rezende CMF, Silva MR, Pêgo AP, Borges O, Goes AM. A new strategy based on Smrho protein loaded chitosan nanoparticles as a candidate oral vaccine against schistosomiasis. PLoS Negl Trop Dis. 2012;6(11):e1894. https://doi.org/10.1371/journal.pntd.0001894.

    Article  PubMed  PubMed Central  Google Scholar 

  211. 211.

    Cambridge CD, Singh SR, Waffo AB, Fairley SJ, Dennis VA. Formulation, characterization, and expression of a recombinant MOMP chlamydia trachomatis DNA vaccine encapsulated in chitosan nanoparticles. Int J Nanomedicine. 2013;8(1):1759–71. https://doi.org/10.2147/ijn.s42723.

    Article  PubMed  PubMed Central  Google Scholar 

  212. 212.

    Sarwar HS, Sohail MF, Saljoughian N, Rehman AU, Akhtar S, Nadhman A, et al. Design of mannosylated oral amphotericin B nanoformulation: efficacy and safety in visceral leishmaniasis. Artif Cells Nanomed Biotechnol. 2018;46(sup1):521–31. https://doi.org/10.1080/21691401.2018.1430699.

    CAS  Article  PubMed  Google Scholar 

  213. 213.

    Das S, Ghosh S, De AK, Bera T. Oral delivery of ursolic acid-loaded nanostructured lipid carrier coated with chitosan oligosaccharides: development, characterization, in vitro and in vivo assessment for the therapy of leishmaniasis. Int J Biol Macromol. 2017;102:996–1008. https://doi.org/10.1016/j.ijbiomac.2017.04.098.

    CAS  Article  PubMed  Google Scholar 

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Şenel, S., Yüksel, S. Chitosan-based particulate systems for drug and vaccine delivery in the treatment and prevention of neglected tropical diseases. Drug Deliv. and Transl. Res. (2020). https://doi.org/10.1007/s13346-020-00806-4

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Keywords

  • Chitosan
  • Neglected tropical disease
  • Drug
  • Vaccine
  • Particulate systems