Advanced search
Publication Cover
Expert Review of Vaccines Volume 11, 2012 - Issue 9
Submit an article Journal homepage
175
Views
8
CrossRef citations to date
0
Altmetric
Review

Plasmodium falciparum malaria vaccines: current status, pitfalls and future directions

Aiala Salvador NanoBioCel Group, Laboratory of Pharmaceutics, University of the Basque Country, School of Pharmacy, Paseo de la Universidad, Vitoria, Spain; Biomedical Research Networking Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Vitoria, Spain; NanoBioCel Group, Laboratory of Pharmaceutics, University of the Basque Country, School of Pharmacy, Paseo de la Universidad, Vitoria, Spain; Biomedical Research Networking Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Vitoria, Spain
,
Rosa M Hernández NanoBioCel Group, Laboratory of Pharmaceutics, University of the Basque Country, School of Pharmacy, Paseo de la Universidad, Vitoria, Spain; Biomedical Research Networking Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Vitoria, Spain; NanoBioCel Group, Laboratory of Pharmaceutics, University of the Basque Country, School of Pharmacy, Paseo de la Universidad, Vitoria, Spain; Biomedical Research Networking Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Vitoria, Spain
,
José Luis Pedraz NanoBioCel Group, Laboratory of Pharmaceutics, University of the Basque Country, School of Pharmacy, Paseo de la Universidad, Vitoria, Spain; Biomedical Research Networking Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Vitoria, Spain; NanoBioCel Group, Laboratory of Pharmaceutics, University of the Basque Country, School of Pharmacy, Paseo de la Universidad, Vitoria, Spain; Biomedical Research Networking Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Vitoria, Spain
&
Manoli Igartua NanoBioCel Group, Laboratory of Pharmaceutics, University of the Basque Country, School of Pharmacy, Paseo de la Universidad, Vitoria, Spain; Biomedical Research Networking Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Vitoria, Spain; NanoBioCel Group, Laboratory of Pharmaceutics, University of the Basque Country, School of Pharmacy, Paseo de la Universidad, Vitoria, Spain. [email protected]
Pages 1071-1086 | Published online: 09 Jan 2014

References

  • Price RN, Douglas NM, Anstey NM. New developments in Plasmodium vivax malaria: severe disease and the rise of chloroquine resistance. Curr. Opin. Infect. Dis. 22(5), 430–435 (2009).
  • Sauerwein RW. Clinical malaria vaccine development. Immunol. Lett. 122(2), 115–117 (2009).
  • Nardin E. The past decade in malaria synthetic peptide vaccine clinical trials. Hum. Vaccin. 6(1), 27–38 (2010).
  • Hoffman SL, Goh LM, Luke TC et al. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J. Infect. Dis. 185(8), 1155–1164 (2002).
  • Nussenzweig RS, Vanderberg J, Most H, Orton C. Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. Nature 216(5111), 160–162 (1967).
  • Hoffman SL, Billingsley PF, James E et al. Development of a metabolically active, non-replicating sporozoite vaccine to prevent Plasmodium falciparum malaria. Hum. Vaccin. 6(1), 97–106 (2010).
  • Voza T, Kebaier C, Vanderberg JP. Intradermal immunization of mice with radiation-attenuated sporozoites of Plasmodium yoelii induces effective protective immunity. Malar. J. 9, 362 (2010).
  • Epstein JE, Tewari K, Lyke KE et al. Live attenuated malaria vaccine designed to protect through hepatic CD8+ T cell immunity. Science 334(6055), 475–480 (2011).
  • Kumar KA, Baxter P, Tarun AS, Kappe SH, Nussenzweig V. Conserved protective mechanisms in radiation and genetically attenuated uis3(-) and uis4(-) Plasmodium sporozoites. PLoS ONE 4(2), e4480 (2009).
  • Douradinha B, van Dijk MR, Ataide R et al. Genetically attenuated P36p-deficient Plasmodium berghei sporozoites confer long-lasting and partial cross-species protection. Int. J. Parasitol. 37(13), 1511–1519 (2007).
  • van Schaijk BC, Janse CJ, van Gemert GJ et al. Gene disruption of Plasmodium falciparum p52 results in attenuation of malaria liver stage development in cultured primary human hepatocytes. PLoS ONE 3(10), e3549 (2008).
  • Butler NS, Schmidt NW, Vaughan AM, Aly AS, Kappe SH, Harty JT. Superior antimalarial immunity after vaccination with late liver stage-arresting genetically attenuated parasites. Cell Host Microbe 9(6), 451–462 (2011).
  • Hill AV. Vaccines against malaria. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366(1579), 2806–2814 (2011).
  • Annoura T, Ploemen IH, van Schaijk BC et al. Assessing the adequacy of attenuation of genetically modified malaria parasite vaccine candidates. Vaccine 30(16), 2662–2670 (2012).
  • Butler NS, Vaughan AM, Harty JT, Kappe SH. Whole parasite vaccination approaches for prevention of malaria infection. Trends Immunol. 33(5), 247–254 (2012).
  • Purcell LA, Yanow SK, Lee M, Spithill TW, Rodriguez A. Chemical attenuation of Plasmodium berghei sporozoites induces sterile immunity in mice. Infect. Immun. 76(3), 1193–1199 (2008).
  • Pinder M, Moorthy VS, Akanmori BD, Genton B, Brown GV. MALVAC 2009: progress and challenges in development of whole organism malaria vaccines for endemic countries, 3–4 June 2009, Dakar, Senegal. Vaccine 28(30), 4695–4702 (2010).
  • Guilbride DL, Gawlinski P, Guilbride PD. Why functional pre-erythrocytic and bloodstage malaria vaccines fail: a meta-analysis of fully protective immunizations and novel immunological model. PLoS ONE 5(5), e10685 (2010).
  • Anders RF. The case for a subunit vaccine against malaria. Trends Parasitol. 27(8), 330–334 (2011).
  • Kennedy MC, Wang J, Zhang Y et al. In vitro studies with recombinant Plasmodium falciparum apical membrane antigen 1 (AMA1): production and activity of an AMA1 vaccine and generation of a multiallelic response. Infect. Immun. 70(12), 6948–6960 (2002).
  • Pombo DJ, Lawrence G, Hirunpetcharat C et al. Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum. Lancet 360(9333), 610–617 (2002).
  • Pinzon-Charry A, McPhun V, Kienzle V et al. Low doses of killed parasite in CpG elicit vigorous CD4+ T cell responses against blood-stage malaria in mice. J. Clin. Invest. 120(8), 2967–2978 (2010).
  • Friesen J, Silvie O, Putrianti ED, Hafalla JC, Matuschewski K, Borrmann S. Natural immunization against malaria: causal prophylaxis with antibiotics. Sci. Transl. Med. 2(40), 40ra49 (2010).
  • Roestenberg M, McCall M, Hopman J et al. Protection against a malaria challenge by sporozoite inoculation. N. Engl. J. Med. 361(5), 468–477 (2009).
  • Roestenberg M, Teirlinck AC, McCall MB et al. Long-term protection against malaria after experimental sporozoite inoculation: an open-label follow-up study. Lancet 377(9779), 1770–1776 (2011).
  • Muregi FW, Kirira PG, Ishih A. Novel rational drug design strategies with potential to revolutionize malaria chemotherapy. Curr. Med. Chem. 18(1), 113–143 (2011).
  • Friesen J, Matuschewski K. Comparative efficacy of pre-erythrocytic whole organism vaccine strategies against the malaria parasite. Vaccine 29(40), 7002–7008 (2011).
  • Nussenzweig RS, Vanderberg J, Spitalny GL, Rivera CI, Orton C, Most H. Sporozoite-induced immunity in mammalian malaria. A review. Am. J. Trop. Med. Hyg. 21(5), 722–728 (1972).
  • Trieu A, Kayala MA, Burk C et al. Sterile protective immunity to malaria is associated with a panel of novel P. falciparum antigens. Mol. Cell. Proteomics 10(9), M111.007948 (2011).
  • Montero Vega MT. A new era for innate immunity. Allergol. Immunopathol. (Madr.) 36(3), 164–175 (2008).
  • Tewari K, Flynn BJ, Boscardin SB et al. Poly(I:C) is an effective adjuvant for antibody and multi-functional CD4+ T cell responses to Plasmodium falciparum circumsporozoite protein (CSP) and αDEC-CSP in non human primates. Vaccine 28(45), 7256–7266 (2010).
  • Salaun B, Greutert M, Romero P. Toll-like receptor 3 is necessary for dsRNA adjuvant effects. Vaccine 27(12), 1841–1847 (2009).
  • Schwartz KL, Brown GV, Genton B, Moorthy VS. A review of malaria vaccine projects based on the WHO rainbow table. Malar J. 11, 11 (2012).
  • Nardin EH, Oliveira GA, Calvo-Calle JM et al. Phase I testing of a malaria vaccine composed of hepatitis B virus core particles expressing Plasmodium falciparum circumsporozoite epitopes. Infect. Immun. 72(11), 6519–6527 (2004).
  • Duncan CJ, Sheehy SH, Ewer KJ et al. Impact on malaria parasite multiplication rates in infected volunteers of the protein-in-adjuvant vaccine AMA1-C1/Alhydrogel+CPG 7909. PLoS ONE 6(7), e22271 (2011).
  • Salvador A, Igartua M, Hernández RM, Pedraz JL. Combination of immune stimulating adjuvants with poly(lactide-co-glycolide) microspheres enhances the immune response of vaccines. Vaccine 30(3), 589–596 (2012).
  • Birkett A, Lyons K, Schmidt A et al. A modified hepatitis B virus core particle containing multiple epitopes of the Plasmodium falciparum circumsporozoite protein provides a highly immunogenic malaria vaccine in preclinical analyses in rodent and primate hosts. Infect. Immun. 70(12), 6860–6870 (2002).
  • Gregson AL, Oliveira G, Othoro C et al. Phase I trial of an alhydrogel adjuvanted hepatitis B core virus-like particle containing epitopes of Plasmodium falciparum circumsporozoite protein. PLoS ONE 3(2), e1556 (2008).
  • Böttcher B, Wynne SA, Crowther RA. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386(6620), 88–91 (1997).
  • Oliveira GA, Wetzel K, Calvo-Calle JM et al. Safety and enhanced immunogenicity of a hepatitis B core particle Plasmodium falciparum malaria vaccine formulated in adjuvant Montanide ISA 720 in a Phase I trial. Infect. Immun. 73(6), 3587–3597 (2005).
  • Walther M, Dunachie S, Keating S et al. Safety, immunogenicity and efficacy of a pre-erythrocytic malaria candidate vaccine, ICC-1132 formulated in Seppic ISA 720. Vaccine 23(7), 857–864 (2005).
  • Garçon N, Van Mechelen M. Recent clinical experience with vaccines using MPL- and QS-21-containing adjuvant systems. Expert Rev. Vaccines 10(4), 471–486 (2011).
  • Casares S, Brumeanu TD, Richie TL. The RTS,S malaria vaccine. Vaccine 28(31), 4880–4894 (2010).
  • Kester KE, Cummings JF, Ofori-Anyinam O et al .; RTS,S Vaccine Evaluation Group. Randomized, double-blind, Phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. J. Infect. Dis. 200(3), 337–346 (2009).
  • Polhemus ME, Remich SA, Ogutu BR et al. Evaluation of RTS,S/AS02A and RTS,S/AS01B in adults in a high malaria transmission area. PLoS ONE 4(7), e6465 (2009).
  • Asante KP, Abdulla S, Agnandji S et al. Safety and efficacy of the RTS,S/AS01E candidate malaria vaccine given with expanded-programme-on-immunisation vaccines: 19 month follow-up of a randomised, open-label, Phase 2 trial. Lancet Infect. Dis. 11(10), 741–749 (2011).
  • Leach A, Vekemans J, Lievens M et al . Clinical Trials Partnership Committee. Design of a Phase III multicenter trial to evaluate the efficacy of the RTS,S/AS01 malaria vaccine in children across diverse transmission settings in Africa. Malar. J. 10, 224 (2011).
  • Vekemans J, Marsh K, Greenwood B et al . Clinical Trials Partnership Committee. Assessment of severe malaria in a multicenter, Phase III, RTS,S/AS01 malaria candidate vaccine trial: case definition, standardization of data collection and patient care. Malar. J. 10, 221 (2011).
  • Selidji TA, Bertrand L, Solange SS et al. First results of Phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N. Engl. J. Med. 365(20), 1863–1875 (2011).
  • Ballou WR, Arevalo-Herrera M, Carucci D et al. Update on the clinical development of candidate malaria vaccines. Am. J. Trop. Med. Hyg. 71(Suppl. 2), 239–247 (2004).
  • Salvador A, Igartua M, Hernández RM, Pedraz JL. An overview on the field of micro- and nanotechnologies for synthetic peptide-based vaccines. J. Drug Deliv. 2011, 1–18 (2011).
  • Men Y, Tamber H, Audran R, Gander B, Corradin G. Induction of a cytotoxic T lymphocyte response by immunization with a malaria specific CTL peptide entrapped in biodegradable polymer microspheres. Vaccine 15(12–13), 1405–1412 (1997).
  • Patarroyo ME, Amador R, Clavijo P et al. A synthetic vaccine protects humans against challenge with asexual blood stages of Plasmodium falciparum malaria. Nature 332(6160), 158–161 (1988).
  • Graves P, Gelband H. Vaccines for preventing malaria (blood-stage). Cochrane Database Syst. Rev. 4, CD006199 (2006).
  • Igartua M, Hernández RM, Rosas JE, Patarroyo ME, Pedraz JL. Gamma-irradiation effects on biopharmaceutical properties of PLGA microspheres loaded with SPf66 synthetic vaccine. Eur. J. Pharm. Biopharm. 69(2), 519–526 (2008).
  • Rosas JE, Hernández RM, Gascón AR et al. Biodegradable PLGA microspheres as a delivery system for malaria synthetic peptide SPf66. Vaccine 19(31), 4445–4451 (2001).
  • Rosas JE, Pedraz JL, Hernández RM et al. Remarkably high antibody levels and protection against P. falciparum malaria in Aotus monkeys after a single immunisation of SPf66 encapsulated in PLGA microspheres. Vaccine 20(13–14), 1707–1710 (2002).
  • Carcaboso AM, Hernández RM, Igartua M et al. Immune response after oral administration of the encapsulated malaria synthetic peptide SPf66. Int. J. Pharm. 260(2), 273–282 (2003).
  • Carcaboso AM, Hernández RM, Igartua M, Rosas JE, Patarroyo ME, Pedraz JL. Potent, long lasting systemic antibody levels and mixed Th1/Th2 immune response after nasal immunization with malaria antigen loaded PLGA microparticles. Vaccine 22(11–12), 1423–1432 (2004).
  • Carcaboso AM, Hernández RM, Igartua M, Rosas JE, Patarroyo ME, Pedraz JL. Enhancing immunogenicity and reducing dose of microparticulated synthetic vaccines: single intradermal administration. Pharm. Res. 21(1), 121–126 (2004).
  • Mata E, Igartua M, Patarroyo ME, Pedraz JL, Hernández RM. Enhancing immunogenicity to PLGA microparticulate systems by incorporation of alginate and RGD-modified alginate. Eur. J. Pharm. Sci. 44(1–2), 32–40 (2011).
  • Anderson RJ, Hannan CM, Gilbert SC et al. Enhanced CD8+ T cell immune responses and protection elicited against Plasmodium berghei malaria by prime boost immunization regimens using a novel attenuated fowlpox virus. J. Immunol. 172(5), 3094–3100 (2004).
  • Gilbert SC, Schneider J, Hannan CM et al. Enhanced CD8 T cell immunogenicity and protective efficacy in a mouse malaria model using a recombinant adenoviral vaccine in heterologous prime–boost immunisation regimes. Vaccine 20(7–8), 1039–1045 (2002).
  • Reyes-Sandoval A, Berthoud T, Alder N et al. Prime–boost immunization with adenoviral and modified vaccinia virus Ankara vectors enhances the durability and polyfunctionality of protective malaria CD8+ T-cell responses. Infect. Immun. 78(1), 145–153 (2010).
  • Webster DP, Dunachie S, Vuola JM et al. Enhanced T cell-mediated protection against malaria in human challenges by using the recombinant poxviruses FP9 and modified vaccinia virus Ankara. Proc. Natl. Acad. Sci. USA 102(13), 4836–4841 (2005).
  • O’Hara GA, Duncan CJ, Ewer KJ et al. Clinical assessment of a recombinant simian adenovirus ChAd63: a potent new vaccine vector. J. Infect. Dis. 205(5), 772–781 (2012).
  • Geels MJ, Imoukhuede EB, Imbault N et al. European vaccine initiative: lessons from developing malaria vaccines. Expert Rev. Vaccines 10(12), 1697–1708 (2011).
  • Sheehy SH, Duncan CJ, Elias SC et al. Phase Ia clinical evaluation of the Plasmodium falciparum blood-stage antigen MSP1 in ChAd63 and MVA vaccine vectors. Mol. Ther. 19(12), 2269–2276 (2011).
  • Porter DW, Thompson FM, Berthoud TK et al. A human Phase I/IIa malaria challenge trial of a polyprotein malaria vaccine. Vaccine 29(43), 7514–7522 (2011).
  • Radosevic K, Rodriguez A, Lemckert AA et al. The Th1 immune response to Plasmodium falciparum circumsporozoite protein is boosted by adenovirus vectors 35 and 26 with a homologous insert. Clin. Vaccine Immunol. 17(11), 1687–1694 (2010).
  • Dunachie SJ, Walther M, Vuola JM et al. A clinical trial of prime–boost immunisation with the candidate malaria vaccines RTS,S/AS02A and MVA-CS. Vaccine 24(15), 2850–2859 (2006).
  • Cummings JF, Spring MD, Schwenk RJ et al. Recombinant liver stage antigen-1 (LSA-1) formulated with AS01 or AS02 is safe, elicits high titer antibody and induces IFN-gamma/IL-2 CD4+ T cells but does not protect against experimental Plasmodium falciparum infection. Vaccine 28(31), 5135–5144 (2010).
  • Spring MD, Cummings JF, Ockenhouse CF et al. Phase 1/2a study of the malaria vaccine candidate apical membrane antigen-1 (AMA-1) administered in adjuvant system AS01B or AS02A. PLoS ONE 4(4), e5254 (2009).
  • Okitsu SL, Mueller MS, Amacker M et al. Preclinical profiling of the immunogenicity of a two-component subunit malaria vaccine candidate based on virosome technology. Hum. Vaccin. 4(2), 106–114 (2008).
  • Genton B, Pluschke G, Degen L et al. A randomized placebo-controlled Phase Ia malaria vaccine trial of two virosome-formulated synthetic peptides in healthy adult volunteers. PLoS ONE 2(10), e1018 (2007).
  • Thompson FM, Porter DW, Okitsu SL et al. Evidence of blood stage efficacy with a virosomal malaria vaccine in a Phase IIa clinical trial. PLoS ONE 3(1), e1493 (2008).
  • Cech PG, Aebi T, Abdallah MS et al. Virosome-formulated Plasmodium falciparum AMA-1 & CSP derived peptides as malaria vaccine: randomized Phase 1b trial in semi-immune adults & children. PLoS ONE 6(7), e22273 (2011).
  • Esen M, Kremsner PG, Schleucher R et al. Safety and immunogenicity of GMZ2 – a MSP3–GLURP fusion protein malaria vaccine candidate. Vaccine 27(49), 6862–6868 (2009).
  • Mordmüller B, Szywon K, Greutelaers B et al. Safety and immunogenicity of the malaria vaccine candidate GMZ2 in malaria-exposed, adult individuals from Lambaréné, Gabon. Vaccine 28(41), 6698–6703 (2010).
  • Bélard S, Issifou S, Hounkpatin AB et al. A randomized controlled Phase Ib trial of the malaria vaccine candidate GMZ2 in African children. PLoS ONE 6(7), e22525 (2011).
  • Horii T, Shirai H, Jie L et al. Evidences of protection against blood-stage infection of Plasmodium falciparum by the novel protein vaccine SE36. Parasitol. Int. 59(3), 380–386 (2010).
  • El Sahly HM, Patel SM, Atmar RL et al. Safety and immunogenicity of a recombinant nonglycosylated erythrocyte binding antigen 175 Region II malaria vaccine in healthy adults living in an area where malaria is not endemic. Clin. Vaccine Immunol. 17(10), 1552–1559 (2010).
  • López JA, Weilenman C, Audran R et al. A synthetic malaria vaccine elicits a potent CD8(+) and CD4(+) T lymphocyte immune response in humans. Implications for vaccination strategies. Eur. J. Immunol. 31(7), 1989–1998 (2001).
  • Audran R, Lurati-Ruiz F, Genton B et al. The synthetic Plasmodium falciparum circumsporozoite peptide PfCS102 as a malaria vaccine candidate: a randomized controlled Phase I trial. PLoS ONE 4(10), e7304 (2009).
  • Genton B, D’Acremont V, Lurati-Ruiz F et al. Randomized double-blind controlled Phase I/IIa trial to assess the efficacy of malaria vaccine PfCS102 to protect against challenge with P. falciparum. Vaccine 28(40), 6573–6580 (2010).
  • Malkin E, Hu J, Li Z et al. A Phase 1 trial of PfCP2.9: an AMA1/MSP1 chimeric recombinant protein vaccine for Plasmodium falciparum malaria. Vaccine 26(52), 6864–6873 (2008).
  • Ogutu BR, Apollo OJ, McKinney D et al .; MSP-1 Malaria Vaccine Working Group. Blood stage malaria vaccine eliciting high antigen-specific antibody concentrations confers no protection to young children in Western Kenya. PLoS ONE 4(3), e4708 (2009).
  • Yimin W, Ellis RD, Shaffer D et al. Phase 1 trial of malaria transmission blocking vaccine candidates Pfs25 and Pvs25 formulated with montanide ISA 51. PLoS ONE 3(7), e2636 (2008).
  • Dunachie SJ, Walther M, Epstein JE et al. A DNA prime-modified vaccinia virus ankara boost vaccine encoding thrombospondin-related adhesion protein but not circumsporozoite protein partially protects healthy malaria-naive adults against Plasmodium falciparum sporozoite challenge. Infect. Immun. 74(10), 5933–5942 (2006).
  • Wang R, Epstein J, Charoenvit Y et al. Induction in humans of CD8+ and CD4+ T cell and antibody responses by sequential immunization with malaria DNA and recombinant protein. J. Immunol. 172(9), 5561–5569 (2004).
  • Epstein JE, Charoenvit Y, Kester KE et al. Safety, tolerability, and antibody responses in humans after sequential immunization with a PfCSP DNA vaccine followed by the recombinant protein vaccine RTS,S/AS02A. Vaccine 22(13–14), 1592–1603 (2004).
  • Takala SL, Plowe CV. Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming ‘vaccine resistant malaria’. Parasite Immunol. 31(9), 560–573 (2009).
  • Cunnington AJ, Riley EM. Suppression of vaccine responses by malaria: insignificant or overlooked? Expert Rev. Vaccines 9(4), 409–429 (2010).

Patent

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.