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A historical and systematic overview of Ascaris vaccine development

Published online by Cambridge University Press:  09 August 2021

Ana Clara Gazzinelli-Guimarães
Affiliation:
Departamento de Parasitologia, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
Pedro Gazzinelli-Guimarães
Affiliation:
Laboratory of Parasitic Diseases, NIAID, National Institutes of Health, Bethesda, MD, USA
Jill E. Weatherhead*
Affiliation:
Department of Medicine, Infectious Diseases, Baylor College of Medicine, Houston, TX, USA Department of Pediatrics, Pediatric Tropical Medicine, Baylor College of Medicine, Houston, TX, USA National School of Tropical Medicine, Baylor College of Medicine, Houston, TX, USA
*
Author for correspondence: Jill E. Weatherhead, E-mail: [email protected]

Abstract

Ascariasis is the most prevalent helminth infection in the world and leads to significant, life-long morbidity, particularly in young children. Current efforts to control and eradicate ascariasis in endemic regions have been met with significant challenges including high-rates of re-infection and potential development of anthelminthic drug resistance. Vaccines against ascariasis are a key tool that could break the transmission cycle and lead to disease eradication globally. Evolution of the Ascaris vaccine pipeline has progressed, however no vaccine product has been brought to human clinical trials to date. Advancement in recombinant protein technology may provide the first step in generating an Ascaris vaccine as well as a pan-helminthic vaccine ready for human trials. However, several roadblocks remain and investment in new technologies will be important to develop a successful human Ascaris vaccine that is critically needed to prevent significant morbidity in Ascaris-endemic regions around the world.

Type
Review Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Anthony, RM, Rutitzky, LI, Urban, JF Jr, Stadecker, MJ and Gause, WC (2007) Protective immune mechanisms in helminth infection. Nature Reviews Immunology 7, 975987.10.1038/nri2199CrossRefGoogle ScholarPubMed
Arean, VM and Crandall, CA (1962) The effect of immunization on the fate of injected second stage Ascaris lumbricoides larvae in the rabbit. The American Journal of Tropical Medicine and Hygiene 11, 369379.10.4269/ajtmh.1962.11.369CrossRefGoogle ScholarPubMed
Betson, M and Stothard, JR (2016) Ascaris lumbricoides or Ascaris suum: what's in a name?. The Journal of Infectious Diseases 213, 13551356.10.1093/infdis/jiw037CrossRefGoogle ScholarPubMed
Chen, D, Colditz, IG, Glenn, GM and Tsonis, CG (2002) Effect of transcutaneous immunization with co-administered antigen and cholera toxin on systemic and mucosal antibody responses in sheep. Veterinary Immunology and Immunopathology 86, 177182.10.1016/S0165-2427(02)00037-5CrossRefGoogle ScholarPubMed
Chen, N, Yuan, ZG, Xu, MJ, Zhou, DH, Zhang, XX, Zhang, YZ, Wang, XW, Yan, C, Lin, RQ and Zhu, XQ (2012) Ascaris suum enolase is a potential vaccine candidate against ascariasis. Vaccine 30, 34783482.10.1016/j.vaccine.2012.02.075CrossRefGoogle ScholarPubMed
Chico, ME, Vaca, MG, Rodriguez, A and Cooper, PJ (2019) Soil-transmitted helminth parasites and allergy: observations from Ecuador. Parasite Immunology 41, e12590.10.1111/pim.12590CrossRefGoogle ScholarPubMed
Colombo, SAP and Grencis, RK (2020) Immunity to soil-transmitted helminths: evidence from the field and laboratory models. Frontiers in Immunology 11, 1286.10.3389/fimmu.2020.01286CrossRefGoogle ScholarPubMed
Cooper, PJ, Chico, ME, Sandoval, C, Espinel, I, Angel, G, Kennedy, MW, Urban, JF Jr, Griffin, GE and Nutman, T (2000) Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. The Journal of Infectious Diseases 182, 12071213.10.1086/315830CrossRefGoogle ScholarPubMed
Da'dara, AA and Harn, DA (2005) DNA vaccines against tropical parasitic diseases. Expert Review of Vaccines 4, 575589.10.1586/14760584.4.4.575CrossRefGoogle ScholarPubMed
Da Silva Alves, EB, Conceição, MJ and Leles, D (2016) Ascaris lumbricoides, Ascaris suum, or ‘Ascaris lumbrisuum’? Journal of Infectious Diseases 213, 1355.Google ScholarPubMed
de Castro, JC, de Almeida, LV, Cardoso, MS, Oliveira, F, Nogueira, DS, Reis-Cunha, JL, Magalhaes, L, Zhan, B, Bottazzi, ME, Hotez, PJ, Bueno, LL, Bartholomeu, DC and Fujiwara, RT (2021) Vaccination with chimeric protein induces protection in murine model against ascariasis. Vaccine 39, 394401.10.1016/j.vaccine.2020.11.046CrossRefGoogle ScholarPubMed
de Silva, NR, Guyatt, HL and Bundy, DA (1997) Morbidity and mortality due to Ascaris-induced intestinal obstruction. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 3136.10.1016/S0035-9203(97)90384-9CrossRefGoogle ScholarPubMed
Diemert, DJ, Pinto, AG, Freire, J, Jariwala, A, Santiago, H, Hamilton, RG, Periago, MV, Loukas, A, Tribolet, L, Mulvenna, J, Correa-Oliveira, R, Hotez, PJ and Bethony, JM (2012) Generalized urticaria induced by the Na-ASP-2 hookworm vaccine: implications for the development of vaccines against helminths. Journal of Allergy and Clinical Immunology 130, 169–76.e6.10.1016/j.jaci.2012.04.027CrossRefGoogle ScholarPubMed
Disease, G. B. of (2020) Ascariasis – Level 4 cause. Institute for Health Metrics and Evaluation. http://www.healthdata.org/results/gbd_summaries/2019/ascariasis-level-4-cause.Google Scholar
Ezeamama, AE, Friedman, JF, Acosta, LP, Bellinger, DC, Langdon, GC, Manalo, DL, Olveda, RM, Kurtis, JD and McGarvey, ST (2005) Helminth infection and cognitive impairment among Filipino children. American Journal of Tropical Medicine and Hygiene 72, 540548.10.4269/ajtmh.2005.72.540CrossRefGoogle ScholarPubMed
Farrell, SH, Coffeng, LE, Truscott, JE, Werkman, M, Toor, J, de Vlas, SJ and Anderson, RM (2018) Investigating the effectiveness of current and modified world health organization guidelines for the control of soil-transmitted helminth infections. Clinical Infectious Diseases 66, S253S259.10.1093/cid/ciy002CrossRefGoogle ScholarPubMed
Frontera, E, Carrón, A, Serrano, FJ, Roepstorff, A, Reina, D and Navarrete, I (2003) Specific systemic IgG1, IgG2 and IgM responses in pigs immunized with infective eggs or selected antigens of Ascaris suum. Parasitology 127, 291298.10.1017/S003118200300355XCrossRefGoogle ScholarPubMed
Furtado, LFV, Medeiros, C, Zuccherato, LW, Alves, WP, de Oliveira, V, da Silva, VJ, Miranda, GS, Fujiwara, RT and Rabelo, É (2019) First identification of the benzimidazole resistance-associated F200Y SNP in the betatubulin gene in Ascaris lumbricoides. PLoS ONE 14, e0224108.10.1371/journal.pone.0224108CrossRefGoogle Scholar
Gazzinelli-Guimaraes, PH and Nutman, TB (2018) Helminth parasites and immune regulation [version 1; peer review: 2 approved]. F1000Research 7, F1000 Faculty Rev-1685.10.12688/f1000research.15596.1CrossRefGoogle Scholar
Gazzinelli-Guimaraes, (2019) Allergen presensitization drives an eosinophil-dependent arrest in lung-specific helminth development. JCI PMID: 31380805.10.1172/JCI127963CrossRefGoogle ScholarPubMed
Gazzinelli-Guimarães, PH, Gazzinelli-Guimarães, AC, Silva, FN, Mati, VL, Dhom-Lemos, L, Barbosa, FS, Passos, LS, Gaze, S, Carneiro, CM, Bartholomeu, DC, Bueno, LL and Fujiwara, RT (2013) Parasitological and immunological aspects of early Ascaris spp. Infection in mice. International Journal for Parasitology 43, 697706.10.1016/j.ijpara.2013.02.009CrossRefGoogle ScholarPubMed
Gazzinelli-Guimarães, AC, Gazzinelli-Guimarães, PH, Nogueira, DS, Oliveira, F, Barbosa, FS, Amorim, C, Cardoso, MS, Kraemer, L, Caliari, MV, Akamatsu, MA, Ho, PL, Jones, KM, Weatherhead, J, Bottazzi, ME, Hotez, PJ, Zhan, B, Bartholomeu, DC, Russo, RC, Bueno, LL and Fujiwara, RT (2018) IgG induced by vaccination with Ascaris suum extracts is protective against infection. Frontiers in Immunology 9, 2535.10.3389/fimmu.2018.02535CrossRefGoogle ScholarPubMed
Girasol, MJ, Grecia, LR, Fabi, JC, Fernandez, AJ, Isabela Fernandez, JN, Flores, G, Flores, R, Fontanilla, EL, Fragante, PJ, Genuino, VC, Go, SC, Gotico, I, Gregorio, ME, Griño, MA, Guevarra, PM, Guinal, S, Guldam, R, Infante, GC, Jalandoni, JP, Juyad, IG and Manglicmot-Yabes, A (2021) Evaluation of crude adult Ascaris suum intestinal tract homogenate in inducing protective IgG production against A. suum larvae in BALB/c mice. Experimental Parasitology 221, 108049.10.1016/j.exppara.2020.108049CrossRefGoogle ScholarPubMed
Hill, DE, Fetterer, RH, Romanowski, RD and Urban, JF (1994) The effect of immunization of pigs with Ascaris suum cuticle components on the development of resistance to parenteral migration during a challenge infection. Veterinary Immunology and Immunopathology 42, 161169.10.1016/0165-2427(94)90005-1CrossRefGoogle ScholarPubMed
Hotez, PJ and Booker, C (2020) STOP: study, treat, observe, and prevent neglected diseases of poverty act. PLoS Neglected Tropical Diseases 14, e0008064.10.1371/journal.pntd.0008064CrossRefGoogle ScholarPubMed
Islam, MK, Miyoshi, T and Tsuji, N (2005 b) Vaccination with recombinant Ascaris suum 24-kilodalton antigen induces a Th1/Th2-mixed type immune response and confers high levels of protection against challenged Ascaris suum lung-stage infection in BALB/c mice. International Journal for Parasitology 35, 10231030.10.1016/j.ijpara.2005.03.019CrossRefGoogle ScholarPubMed
Islam, MK, et al. (2005 a) Pyrophosphatase of the roundworm Ascaris suum plays an essential role in the worm's molting and development. Infection and Immunity 73, 19952004.10.1128/IAI.73.4.1995-2004.2005CrossRefGoogle ScholarPubMed
Jia, T-W, Melville, S, Utzinger, J, King, CH and Zhou, XN (2012) Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis. PLoS Neglected Tropical Diseases 6, e1621.10.1371/journal.pntd.0001621CrossRefGoogle ScholarPubMed
Jourdan, PM, Lamberton, P, Fenwick, A and Addiss, DG (2018) Soil-transmitted helminth infections. The Lancet 391, 252265.10.1016/S0140-6736(17)31930-XCrossRefGoogle ScholarPubMed
Leles, D, Gardner, SL, Reinhard, K, Iñiguez, A and Araujo, A (2012) Are Ascaris lumbricoides and Ascaris suum a single species? Parasites & Vectors 5, 42.10.1186/1756-3305-5-42CrossRefGoogle ScholarPubMed
Lewis, R, Behnke, JM, Stafford, P and Holland, CV (2005) The development of a mouse model to explore resistance and susceptibility to early Ascaris suum infection. Parasitology 132, 289300.10.1017/S0031182005008978CrossRefGoogle ScholarPubMed
Lewis, R, Behnke, JM, Cassidy, JP, Stafford, P, Murray, N and Holland, CV (2007) The migration of Ascaris suum larvae, and the associated pulmonary inflammatory response in susceptible C57BL/6j and resistant CBA/Ca mice. Parasitology 134, 13011314.10.1017/S0031182007002582CrossRefGoogle ScholarPubMed
Liu, G-H, Wu, CY, Song, HQ, Wei, SJ, Xu, MJ, Lin, RQ, Zhao, GH, Huang, SY and Zhu, XQ (2012) Comparative analyses of the complete mitochondrial genomes of Ascaris lumbricoides and Ascaris suum from humans and pigs. Gene 492, 110116.10.1016/j.gene.2011.10.043CrossRefGoogle ScholarPubMed
Lukes, S (1992) Ascaris suum – vaccination of mice with liposome encapsulated antigen. Veterinary Parasitology 43, 105113.10.1016/0304-4017(92)90053-CCrossRefGoogle ScholarPubMed
Magalhães, L, Nogueira, DS, Gazzinelli-Guimarães, PH, Oliveira, F, Kraemer, L, Gazzinelli-Guimarães, AC, Vieira-Santos, F, Fujiwara, RT and Bueno, LL (2021) Immunological underpinnings of Ascaris infection, reinfection and co-infection and their associated co-morbidities. Parasitology 110. Advance online publication.Google ScholarPubMed
Masure, D, Vlaminck, J, Wang, T, Chiers, K, Van den Broeck, W, Vercruysse, J and Vercruysse, P (2013 a) A role for eosinophils in the intestinal immunity against infective Ascaris suum larvae. PLoS Neglected Tropical Diseases 7, e2138.10.1371/journal.pntd.0002138CrossRefGoogle ScholarPubMed
Masure, D, Wang, T, Vlaminck, J, Claerhoudt, S, Chiers, K, Van den Broeck, W, Saunders, J, Vercruysse, J and Geldhof, P (2013b) The intestinal expulsion of the roundworm Ascaris suum is associated with eosinophils, intra-epithelial T cells and decreased intestinal transit time. PLoS Neglected Tropical Diseases 7, e2588.10.1371/journal.pntd.0002588CrossRefGoogle Scholar
Matsumoto, Y, Suzuki, S, Nozoye, T, Yamakawa, T, Takashima, Y, Arakawa, T, Tsuji, N, Takaiwa, F and Hayashi, Y (2009) Oral immunogenicity and protective efficacy in mice of transgenic rice plants producing a vaccine candidate antigen (As16) of Ascaris suum fused with cholera toxin B subunit. Transgenic Research 18, 185192.10.1007/s11248-008-9205-4CrossRefGoogle ScholarPubMed
Mekonnen, GG, Pearson, M, Loukas, A and Sotillo, J (2018) Extracellular vesicles from parasitic helminths and their potential utility as vaccines. Expert Review of Vaccines 17, 197205.10.1080/14760584.2018.1431125CrossRefGoogle ScholarPubMed
Miller, LA, Colby, K, Manning, SE, Hoenig, D, McEvoy, E, Montgomery, S, Mathison, B, de Almeida, M, Bishop, H, Dasilva, A and Sears, S (2015) Ascariasis in humans and pigs on small-scale farms, Maine, USA, 2010–2013. Emerging Infectious Diseases 21, 332334.10.3201/eid2102.140048CrossRefGoogle Scholar
Mishra, P, Agrawal, A, Joshi, M, Sanghvi, B, Shah, H and Parelkar, SV (2008) Intestinal obstruction in children due to ascariasis: a tertiary health centre experience. African Journal of Paediatric Surgery 5, 6570.10.4103/0189-6725.44178CrossRefGoogle ScholarPubMed
Nogueira, DS, Gazzinelli-Guimarães, PH, Barbosa, FS, Resende, NM, Silva, CC, de Oliveira, LM, Amorim, CC, Oliveira, FM, Mattos, MS, Kraemer, LR, Caliari, MV, Gaze, S, Bueno, LL, Russo, RC and Fujiwara, RT (2016) Multiple exposures to Ascaris suum induce tissue injury and mixed Th2/Th17 immune response in mice. PLoS Neglected Tropical Diseases 10, e0004382.10.1371/journal.pntd.0004382CrossRefGoogle ScholarPubMed
Noon, JB and Aroian, RV (2017) Recombinant subunit vaccines for soil-transmitted helminths. Parasitology 144, 18451870.10.1017/S003118201700138XCrossRefGoogle ScholarPubMed
Oliveira, FMS, da Paixão Matias, PH, Kraemer, L, Gazzinelli-Guimarães, AC, Santos, FV, Amorim, C, Nogueira, DS, Freitas, CS, Caliari, MV, Bartholomeu, DC, Bueno, LL, Russo, RC and Fujiwara, RT (2019) Comorbidity associated to Ascaris suum infection during pulmonary fibrosis exacerbates chronic lung and liver inflammation and dysfunction but not affect the parasite cycle in mice. PLoS Neglected Tropical Diseases 13, e0007896.10.1371/journal.pntd.0007896CrossRefGoogle Scholar
Pabalan, N, Singian, E, Tabangay, L, Jarjanazi, H, Boivin, MJ and Ezeamama, AE (2018) Soil-transmitted helminth infection, loss of education and cognitive impairment in school-aged children: a systematic review and meta-analysis. PLoS Neglected Tropical Diseases 12, e0005523.10.1371/journal.pntd.0005523CrossRefGoogle ScholarPubMed
Peacock, C (2014) Preface.Parasite genomics protocols. Methods in molecular biology (Clifton, N.J.). 1201, v–vi.Google Scholar
Prevention, C.-C. for D. C. and (2015) CDC – Ascariasis – Biology. https://www.cdc.gov/parasites/ascariasis/biology.htmlGoogle Scholar
Rajagopal, S, Hotez, PJ and Bundy, DAP (2014) Micronutrient supplementation and deworming in children with geohelminth infections. PLoS Neglected Tropical Diseases 8, e2920.10.1371/journal.pntd.0002920CrossRefGoogle ScholarPubMed
Rappuoli, R (2000) Reverse vaccinology. Current Opinion in Microbiology 3, 445450.10.1016/S1369-5274(00)00119-3CrossRefGoogle ScholarPubMed
Serrano, FJ, Reina, D, Frontera, E, Roepstorff, A and Navarrete, (2001) Resistance against migrating Ascaris suum larvae in pigs immunized with infective eggs or adult worm antigens. Parasitology 122, 699707.10.1017/S0031182001007806CrossRefGoogle ScholarPubMed
Sette, A and Rappuoli, R (2010) Reverse vaccinology: developing vaccines in the era of genomics. Immunity 33, 530541.10.1016/j.immuni.2010.09.017CrossRefGoogle ScholarPubMed
Shao, CC, Xu, MJ, Alasaad, S, Song, HQ, Peng, L, Tao, JP and Zhu, XQ (2014) Comparative analysis of microRNA profiles between adult Ascaris lumbricoides and Ascaris suum. BMC Veterinary Research 10, 99.10.1186/1746-6148-10-99CrossRefGoogle ScholarPubMed
Soulsby, EJL (1957) Immunization against Ascaris lumbricoides in the Guinea pig. Nature 179, 783784.10.1038/179783a0CrossRefGoogle ScholarPubMed
Sprent, JFA and Chen, HH (1949) Immunological studies in mice infected with the larvae of Ascaris lumbricoides. I. Criteria of immunity and immunizing effect of isolated worm tissues. Journal of Infectious Diseases 84, 111124.10.1093/infdis/84.2.111CrossRefGoogle ScholarPubMed
Starr, MC and Montgomery, SP (2011) Soil-transmitted helminthiasis in the United States: a systematic review – 1940-2010. American Journal of Tropical Medicine and Hygiene 85, 680684.10.4269/ajtmh.2011.11-0214CrossRefGoogle ScholarPubMed
Strunz, EC, Addiss, DG, Stocks, ME, Ogden, S, Utzinger, J and Freeman, MC (2014) Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Medicine 11, e1001620.10.1371/journal.pmed.1001620CrossRefGoogle ScholarPubMed
Taffs, LF (1960) Immunization of guinea pigs against Ascaris suum. Journal of Helminthology 34, 347348.10.1017/S0022149X00021258CrossRefGoogle Scholar
Tromba, FG (1978) Immunization of pigs against experimental Ascaris suum infection by feeding ultraviolet-attenuated eggs. Journal of Parasitology 64, 651656.10.2307/3279954CrossRefGoogle ScholarPubMed
Tsuji, N, Suzuki, K, Kasuga-Aoki, H, Matsumoto, Y, Arakawa, T, Ishiwata, K and Isobe, T (2001) Intranasal immunization with recombinant Ascaris suum 14-kilodalton antigen coupled with cholera toxin B subunit induces protective immunity to A. suum infection in mice. Infection and Immunity 69, 72857292.10.1128/IAI.69.12.7285-7292.2001CrossRefGoogle ScholarPubMed
Tsuji, N, Kasuga-Aoki, H, Isobe, T, Arakawa, T and Matsumoto, Y (2002) Cloning and characterisation of a highly immunoreactive 37 kDa antigen with multiimmunoglobulin domains from the swine roundworm Ascaris suum. International Journal for Parasitology 32, 17391746.10.1016/S0020-7519(02)00179-0CrossRefGoogle ScholarPubMed
Tsuji, N, Suzuki, K, Kasuga-Aoki, H, Isobe, T, Arakawa, T and Matsumoto, Y (2003) Mice intranasally immunized with a recombinant 16-kilodalton antigen from roundworm Ascaris parasites are protected against larval migration of Ascaris suum. Infection and Immunity 71, 53145323.10.1128/IAI.71.9.5314-5323.2003CrossRefGoogle ScholarPubMed
Tsuji, N, Miyoshi, T, Islam, MK, Isobe, T, Yoshihara, S, Arakawa, T, Matsumoto, T and Yokomizo, Y (2004) Recombinant Ascaris 16-kilodalton protein-induced protection against Ascaris suum larval migration after intranasal vaccination in pigs. Journal of Infectious Diseases 190, 18121820.10.1086/425074CrossRefGoogle ScholarPubMed
Urban, JF Jr, and Romanowski, RD (1985) Ascaris suum: protective immunity in pigs immunized with products from eggs and larvae. Experimental parasitology, 60, 245254.10.1016/0014-4894(85)90028-1CrossRefGoogle ScholarPubMed
Urban, JF and Tromba, FG (1982) Development of immune responsiveness to Ascaris suum antigens in pigs vaccinated with ultraviolet-attenuated eggs. Veterinary Immunology and Immunopathology 3, 399409.10.1016/0165-2427(82)90022-8CrossRefGoogle ScholarPubMed
Urban, JR and Tromba, FG (1984) An ultraviolet-attenuated egg vaccine for swine ascariasis: parameters affecting the development of protective immunity. American Journal of Veterinary Research 45, 21042108.Google ScholarPubMed
Urban, JF, Alizadeh, H and Romanowski, RD (1988) Ascaris suum: development of intestinal immunity to infective second-stage larvae in swine. Experimental Parasitology 66, 6677.10.1016/0014-4894(88)90051-3CrossRefGoogle ScholarPubMed
Vaz Nery, S, Pickering, AJ, Abate, E, Asmare, A, Barrett, L, Benjamin-Chung, J, Bundy, D, Clasen, T, Clements, A, Colford, JM, Ercumen, A, Crowley, S, Cumming, O, Freeman, MC, Haque, R, Mengistu, B, Oswald, WE, Pullan, RL, Oliveira, RG, Einterz Owen, K and Brooker, SJ (2019) The role of water, sanitation and hygiene interventions in reducing soil transmitted helminths: interpreting the evidence and identifying next steps. Parasites and Vectors 12, 273.10.1186/s13071-019-3532-6CrossRefGoogle ScholarPubMed
Versteeg, L, Almutairi, MM, Hotez, PJ and Pollet, J (2019) Enlisting the mRNA vaccine platform to combat parasitic infections. Vaccines 7, 122.10.3390/vaccines7040122CrossRefGoogle ScholarPubMed
Versteeg, L, Wei, J, Liu, Z, Keegan, B, Fujiwara, RT, Jones, KM, Asojo, O, Strych, U, Bottazzi, ME, Hotez, PJ and Zhan, B (2020) Protective immunity elicited by the nematode-conserved as37 recombinant protein against Ascaris suum infection. PLoS Neglected Tropical Diseases 14, e0008057.10.1371/journal.pntd.0008057CrossRefGoogle ScholarPubMed
Vlaminck, J, Martinez-Valladares, M, Dewilde, S, Moens, L, Tilleman, K, Deforce, D, Urban, J, Claerebout, E, Vercruysse, J and Geldhof, P (2011) Immunizing pigs with Ascaris suum haemoglobin increases the inflammatory response in the liver but fails to induce a protective immunity. Parasite Immunology 33, 250254.10.1111/j.1365-3024.2010.01274.xCrossRefGoogle ScholarPubMed
Weatherhead, JE (2019) Pediatric Pharmacotherapy: Anthelminthic Treatment. doi: 10.1007/164_2019_254.CrossRefGoogle Scholar
Weatherhead, JE and Hotez, PJ (2015) Worm infections in children. Pediatrics in Review 36, 341352.10.1542/pir.36.8.341CrossRefGoogle ScholarPubMed
Weatherhead, JE, Hotez, PJ and Mejia, R (2017) The global state of helminth control and elimination in children. Pediatric Clinics of North America 64, 867877.10.1016/j.pcl.2017.03.005CrossRefGoogle ScholarPubMed
Weatherhead, JE, Porter, P, Coffey, A, Haydel, D, Versteeg, L, Zhan, B, Gazzinelli Guimarães, AC, Fujiwara, RT, Jaramillo, AM, Bottazzi, ME, Hotez, PJ, Corry, DB and Beaumier, CM (2018) Ascaris larval infection and lung invasion directly induces severe allergic airway disease in mice. Infection and Immunity 86, e00533-18.10.1128/IAI.00533-18CrossRefGoogle Scholar
Weatherhead, JE, Gazzinelli-Guimaraes, PH, Knight, JM, Fujiwara, RT, Hotez, PJ, Bottazzi, ME and Corry, DB (2020) Host immunity and inflammation to pulmonary helminth infections. Frontiers in Immunology 11, 114.10.3389/fimmu.2020.594520CrossRefGoogle ScholarPubMed
Wei, J, Versteeg, L, Liu, Z, Keegan, B, Gazzinelli-Guimarães, AC, Fujiwara, RT, Briggs, N, Jones, KM, Strych, U, Beaumier, CM, Bottazzi, ME, Hotez, PJ and Zhan, B (2017) Yeast-expressed recombinant As16 protects mice against Ascaris suum infection through induction of a Th2-skewed immune response. PLoS Neglected Tropical Diseases 11, e0005769.10.1371/journal.pntd.0005769CrossRefGoogle ScholarPubMed
World Health Organization (2017) Guideline: Preventive chemotherapy to control soil-transmitted helminth infections in at-risk populations groups.Google Scholar
Yamamoto, M, McGhee, JR, Hagiwara, Y, Otake, S and Kiyono, H (2001) Genetically manipulated bacterial toxin as a new generation mucosal adjuvant. Scandinavian Journal of Immunology 53, 211217.10.1046/j.1365-3083.2001.00883.xCrossRefGoogle ScholarPubMed
Zhan, B, Beaumier, CM, Briggs, N, Jones, KM, Keegan, BP, Bottazzi, ME and Hotez, PJ (2014) Advancing a multivalent pan-anthelmintic’ vaccine against soil-transmitted nematode infections. Expert Review of Vaccines 13, 321331.10.1586/14760584.2014.872035CrossRefGoogle ScholarPubMed
Zhou, C, Chen, J, Niu, H, Ouyang, S and Wu, X (2020) Study on the population evolution of Ascaris lumbricoides and Ascaris suum based on whole genome resequencing. Veterinary Parasitology 279, 109062.10.1016/j.vetpar.2020.109062CrossRefGoogle Scholar