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Advancing a Vaccine to Prevent Human Schistosomiasis

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Advancing a Vaccine to Prevent Human Schistosomiasis G Model JVAC 17508 1–4 ARTICLE IN PRESS Vaccine xxx (2016) xxx–xxx Contents lists available at ScienceDirect Vaccine j ournal homepage: www.elsevier.com/locate/vaccine 1 Advancing a vaccine to prevent human schistosomiasis Q1 a,b a,b,c,d,e,f,∗ a,c,d 2 Maureen Merrifield , Peter J. Hotez , Coreen M. Beaumier , a,c,d a,c,d b a,b,c,d,e,f 3 Portia Gillespie , Ulrich Strych , Tara Hayward , Maria Elena Bottazzi a 4 Sabin Vaccine Institute and Texas Children’s Hospital Center for Vaccine Development Houston, TX, USA b 5 Sabin Vaccine Institute, Washington, DC, USA c 6 National School of Tropical Medicine, Baylor College of Medicine, Houston, TX, USA d 7 Department of Pediatrics, Baylor College of Medicine, Houston, TX, USA e 8 Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, TX, USA f 9 Department of Biology, Baylor University, Waco, TX, USA 10 a r a 2211 t i c l e i n f o b s t r a c t 12 13 Article history: Several candidate human schistosomiasis vaccines are in different stages of preclinical and clinical devel- 14 Received 14 August 2015 opment. The major targets are Schistosoma haematobium (urogenitial schistosomiasis) and Schistosoma 15 Accepted 11 March 2016 mansoni (intestinal schistosomiasis) that account for 99% of the world’s 252 million cases, with 90% of 16 Available online xxx these cases in Africa. Two recombinant S. mansoni vaccines – Sm-TSP-2 and Sm-14 are in Phase 1 trials, 17 while Smp80 (calpain) is undergoing testing in non-human primates. Sh28GST, also known as Bilhvax is in 18 Keywords: advanced clinical development for S. haematobium infection. The possibility remains that some of these 19 Schistosomiasis vaccines may cross-react to target both schistosome species. These vaccines were selected on the basis 20 Vaccine of their protective immunity in preclinical challenge models, through human immune-epidemiological 21 Neglected tropical disease studies or both. They are being advanced through a combination of academic research institutions, non- profit vaccine product development partnerships, biotechnology companies, and developing country vaccine manufacturers. In addition, new schistosome candidate vaccines are being identified through bioinformatics, OMICs approaches, and moderate throughput screening, although the full potential of reverse vaccinology for schistosomiasis has not yet been realized. The target product profiles of these vaccines vary but many focus on vaccinating children, in some cases following mass treatment with praz- iquantel, also known as vaccine-linked chemotherapy. Several regulatory pathways have been proposed, some of which rely on World Health Organization prequalification. © 2016 World Health Organization. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/3.0/). 23Q2 Schistosomes are snail-transmitted, water-borne parasitic japonicum or Schistosoma mekongi (the causes of intestinal schis- 36 24 platyhelminthes (order Trematoda) that are found in fresh water tosomiasis in East Asia). Schistosomiasis, together with hookworm 37 25 bodies in low- and middle-income countries. Current estimates and leishmaniasis, rank as those neglected tropical diseases with 38 26 from the Global Burden of Disease Study 2010 (GBD 2010) sug- the highest disease burden as defined by disability-adjusted life 39 27 gest that 252 million people are infected with schistosomes, 90% years (DALYs) [1]. While the GBD 2010 estimated that the world 40 28 of whom live in sub-Saharan Africa [1]. The World Health Orga- lost 3.3 million DALYs from schistosomiasis in 2010 [4], other esti- 41 29 nization (WHO) reports that in 2014 at least 258 million people mates suggest that DALYs lost may even be an order of magnitude 42 30 worldwide required frequent and regular preventive treatment for higher if chronic morbidities such as malnutrition, inflammation, 43 31 schistosomiasis [2]. Recently though, the disease even emerged in and pain are also taken into consideration [5,6]. In addition, there 44 32 Europe on the French island of Corsica [3]. Globally two-thirds of is some evidence that S. haematobium may represent an important 45 33 the cases are infected with Schistosoma haematobium (the cause risk factor for HIV/AIDS acquisition because of the mucosal inflam- 46 34 of urogenital schistosomiasis), one-third with Schistosoma mansoni mation and ulceration caused by genital schistosomiasis in tens of 47 35 (the cause of intestinal schistosomiasis), and 1% with Schistosoma millions of girls and women [7,8]. In addition to S. haematobium- 48 HIV co-infections, S. mansoni and malaria co-infections are also 49 widespread in Africa, and may result in synergistic effects [9]. 50 ∗ Schistosomes reproduce by asexual reproduction in fresh- 51 Corresponding author at: Sabin Vaccine Institute and Texas Children’s Hospital water snails and are released in large numbers as infective 52 Center for Vaccine Development, Houston, TX, USA. E-mail addresses: [email protected], [email protected] (P.J. Hotez). larvae. In water, these cercariae penetrate the skin of a human 53 http://dx.doi.org/10.1016/j.vaccine.2016.03.079 0264-410X/© 2016 World Health Organization. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/3.0/). Please cite this article in press as: Merrifield M, et al. Advancing a vaccine to prevent human schistosomiasis. Vaccine (2016), http://dx.doi.org/10.1016/j.vaccine.2016.03.079 G Model JVAC 17508 1–4 ARTICLE IN PRESS 2 M. Merrifield et al. / Vaccine xxx (2016) xxx–xxx 54 host, transforming into schistosomulae that migrate through the identifying meaningful correlates of immunity, particularly for the 117 55 bloodstream and lungs to the liver where they become adult design of a recombinant immunogen. 118 56 male-female schistosomes. In the host’s mesenteric or bladder 57 venules, the adult schistosomes release their eggs into the tissues 2. General approaches to vaccine development for low- and 119 58 before some make their way into the feces or urine. Upon contact middle-income country markets 120 59 with fresh water, the eggs hatch and give rise to miracidia that 60 enter the intermediate hosts, snails. Schistosomes do not multiply in the human host, and most of 121 61 The pathogenesis of human schistosomiasis begins when eggs the pathology comes as a consequence of the deposition of schisto- 122 62 destined for exit out of the body through feces or urine, instead some eggs in the tissues that lead to end-organ damage associated 123 63 become embedded in the tissues of the human intestine or bladder. with fibrosis, inflammation, and bleeding. Current vaccine develop- 124 64 These trapped eggs subsequently induce inflammation, granulo- ment strategies aim to prevent schistosome infection and/or reduce 125 65 mas, and fibrosis leading to a number of clinical sequelae including ova burden through the interruption of parasite reproduction. Thus, 126 66 hepatic fibrosis and hepatosplenomegaly, hematuria, bladder fibro- among the major vaccine targets are the migrating schistosomulum 127 67 sis and obstruction, hydronephrosis and chronic renal disease. S. stages as well as adult females. 128 68 haematobium ova can also elicit vaginal or cervical inflammation In the 1990s, an independent, WHO/TDR-sponsored evaluation 129 69 (so-called “sandy patches”) that increases the risk of HIV/AIDS of six S. mansoni vaccine candidates in preclinical development 130 70 acquisition, such that schistosomiasis is considered an important found that none achieved better than 40% efficacy in reducing worm 131 71 co-factor in Africa’s AIDS epidemic [7]. Moreover, infection with S. load. 132 72 haematobium is strongly associated with squamous cell carcinoma Since then the maturing of several new technologies, including 133 73 of the bladder [10]. Chronic schistosomiasis, in addition, can lead to OMICs (e.g., genomics, proteomics, transcriptomics), microarrays, 134 74 many other sequelae as well, especially in children, including but and immunomic profiling, have helped in the identification of 135 75 not limited to anemia, chronic pain, undernutrition, growth failure promising new target schistosome antigens [23–25]. However, 136 76 and cognitive deficits [5,6]. both inadequate funding and infrastructure for vaccine devel- 137 77 Strategies to control schistosomiasis center on Mass Drug opment have slowed the translation of these antigen discovery 138 78 Administration (MDA) of an acylated quinoline-pyrazine known as technologies to the clinic. Indeed the overall pipeline of human 139 79 praziquantel (PZQ). While less than 20% of children who need PZQ schistosomiasis vaccines currently in clinical trials is extremely 140 80 MDA actually receive regular treatments, the fact that the preva- modest especially when considering the high disease burden 141 81 lence of schistosomiasis may have increased over the last two to of schistosomiasis and its potential role in Africa’s AIDS epi- 142 82 three decades [11], suggests that MDA with PZQ alone will not be demic. 143 83 adequate for the global elimination of schistosomiasis. Indeed, a For S. haematobium, a single candidate molecule, Sh28GST (Bil- 144 84 survey of almost 400 experts on neglected tropical diseases con- hvax), a schistosome glutathione S-transferase common to the 145 85 cluded that schistosomiasis may not be eliminated through current schistosomula and adult stages, is believed to currently be under- 146 86 approaches [12]. A major reason is that MDA does not interrupt going testing. Early phases 1 and 2 clinical trials conducted in 147 87 transmission and does not prevent schistosome reinfection. With Niger and Senegal have demonstrated an acceptable safety profile 148 88 the added potential for the emergence of PZQ resistance [13,14], and induction of high IgG3 antibody titers that have neutralized 149 89 there is thus an urgent need for vaccines as an alternative approach Sh28GST activity and reduced egg-production, an effect that could 150 90 to lower the disease burden, limit transmission and mitigate the lead to decrease urinary tract pathology and transmission [26,27].
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