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Proteomics of Gnathostomiasis: a Way Forward for Diagnosis and Treatment Development

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Proteomics of Gnathostomiasis: a Way Forward for Diagnosis and Treatment Development pathogens Review Proteomics of Gnathostomiasis: A Way Forward for Diagnosis and Treatment Development Tipparat Thiangtrongjit 1, Kathyleen Nogrado 1, Thawatchai Ketboonlue 2, Preeyarat Malaitong 2, Poom Adisakwattana 2,*,† and Onrapak Reamtong 1,*,† 1 Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand; [email protected] (T.T.); [email protected] (K.N.) 2 Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand; [email protected] (T.K.); [email protected] (P.M.) * Correspondence: [email protected] (P.A.); [email protected] (O.R.) † These two authors contributed equally to this work. Abstract: Gnathostoma spinigerum is the most common cause of gnathostomiasis in humans. It has a complex life cycle, which requires two intermediate hosts and a definitive host, and poses a high risk for zoonosis. Definitive prognosis of gnathostomiasis relies mainly on the isolation of advanced- stage larvae (aL3), which is very challenging especially if the aL3 is sequestered in difficult-to-reach organs. There is also a lack of a confirmatory diagnostic test for gnathostomiasis. With the ongoing advancement of proteomics, a potential diagnostic approach is underway using immunoproteomics and immunodiagnostics. In addition to this, the employment of mass spectrometry could further elucidate not only understanding the biology of the parasite but also determining potential targets Citation: Thiangtrongjit, T.; of prospective drugs and vaccines. This article reports the past, present, and future application of Nogrado, K.; Ketboonlue, T.; proteomics in the study of gnathostomiasis. Malaitong, P.; Adisakwattana, P.; Reamtong, O. Proteomics of Gnathostomiasis: A Way Forward for Keywords: gnathostomiasis; Gnathostoma spinigerum; proteomics; diagnosis; treatment Diagnosis and Treatment Development. Pathogens 2021, 10, 1080. https://doi.org/10.3390/ pathogens10091080 1. Biology and Distribution of Gnathostoma The genus Gnathostoma belongs to the order Spirurida and is one of the groups of Academic Editors: Krystyna parasitic nematodes that prevail in the tropical and subtropical regions. Human gnathosto- Cwiklinski and Mark Robinson miasis is endemic in Southeast Asia (Thailand, Laos, Myanmar, Indonesia, Malaysia, and the Philippines) and Japan, where people eat raw freshwater fish or shellfish [1]. How- Received: 27 July 2021 ever, it is now considered an emerging infectious disease due to increasing occurrence Accepted: 23 August 2021 in non-endemic areas such as Central and South America particularly Mexico [2]. The Published: 25 August 2021 definitive hosts of this parasite are wild and domestic cats, dogs, pigs, rats, and weasels. Currently, a total of 18 species have been described belonging to this genus, but only six Publisher’s Note: MDPI stays neutral species of these are known to infect humans, namely G. binucleatum, G. doloresi, G. bispidum, with regard to jurisdictional claims in G. malaysiae, G. nipponicum, and G. spinigerum, which are geographically distributed in published maps and institutional affil- Asia, Central and South America, Australia, and East Africa [3,4]. Presently, research is iations. needed to improve the diagnosis of gnathostomiasis. Among the previously mentioned human-infecting species of Gnathostoma, G. spinigerum has the most complicated life cycle and poses a higher risk for zoonotic transmission. Thus, it will be given the emphasis in this review [5]. G. spinigerum requires two intermediate hosts and one definitive host Copyright: © 2021 by the authors. to complete its life cycle (Figure1). In general, the adult worms live in the wall of the Licensee MDPI, Basel, Switzerland. stomach of the definitive host (carnivores like canines and felids) and lay eggs, which are This article is an open access article then released into the environment through the feces. The first-stage larvae (L1) hatch from distributed under the terms and the eggs in the freshwater and will be ingested by the first intermediate hosts, copepods conditions of the Creative Commons Attribution (CC BY) license (https:// (usually cyclops species), in which they will develop into second-stage larvae (L2) and creativecommons.org/licenses/by/ early third-stage larvae (eL3). When the second intermediate hosts or paratenic hosts such 4.0/). as fishes, frogs, and snakes ingest the cyclops spp., the eL3 will migrate into the tissue and Pathogens 2021, 10, 1080. https://doi.org/10.3390/pathogens10091080 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, x FOR PEER REVIEW 2 of 10 Pathogens 2021, 10, x FOR PEER REVIEW 2 of 10 Pathogens 2021, 10, 1080 2 of 10 (L2) and early third-stage larvae (eL3). When the second intermediate hosts or paratenic (L2)hosts and such early as fishes,third-stage frogs, larvae and snakes(eL3). When ingest the the second cyclops intermediate spp., the eL3 hosts will or migrate paratenic into thenhoststhe tissue encystsuch andas and fishes, then develop encystfrogs, into andand the snakes develop aL3 (Figureingest into the2theA). cyclopsaL3 In the (Figure casespp., that 2A).the eL3other In thewill paratenic case migrate that hosts, intoother fortheparatenic example,tissue hosts,and reptiles then for encystexample, and birds, and reptiles ingestdevelop theand into secondary bird thes, aL3 ingest intermediate (Figure the secondary2A). hostIn the containing intermediate case that aL3, other host the larvaeparateniccontaining will hosts, notaL3, develop thefor example,larvae further. will reptiles not The develop life and cycle bird fu willrther.s, ingest only The bethe life completed secondary cycle will whenintermediate only thebe completed definitive host hostscontainingwhen (catthe ordefinitive aL3, dog) the ingest larvae hosts the (catwill second or not dog) develop intermediate ingest fu therther. second or The the lifeintermediate paratenic cycle will host oronly harboring the be paratenic completed the aL3.host Thewhenharboring aL3 the could definitive the migrateaL3. The hosts to aL3 the(cat could stomachor dog) migrate ingest and formto the the second the stomach tumor-like intermediate and form mass the ator thethe tumor-like stomachparatenic mass wall host to at mature,harboringthe stomach mate, the wall aL3. and to layThe mature, eggs. aL3 could It mate, is important migrate and lay to to theeggs. note stomach It that is important humans and form are to the accidental note tumor-like that hosts,humans mass as at theare larvaetheaccidental stomach cannot hosts, wall develop asto mature,the in larvae humans mate, cannot and and remain developlay eggs. as in aL3.It humansis However,important and aL3toremain note can that migrateas aL3. humans However, to skin are or visceralaccidentalaL3 can organs,migrate hosts, causing toas skinthe larvaeor severe visceral cannot clinical organs, develop manifestations causing in humans severe [4]. andclinical remain manifestations as aL3. However, [4]. aL3 can migrate to skin or visceral organs, causing severe clinical manifestations [4]. FigureFigure 1.1. TheThe complicated complicated life lifelife cycle cyclecycle of ofof G. G.G. spinigenum spinigenumspinigenum illustrating illustratingillustrating the thethe definitive definitivedefinitive and andand paratenic paratenicparatenic hosts. hosts.hosts. FigureFigure 2.2. PhotoPhoto indicatingindicating the the aL3 aL3 obtain obtainedobtaineded from from the the Asian Asian Asian swamp swamp swamp eels eels eels ( (Monopterus Monopterus(Monopterus albus albus albus))( ()AA ()A) and and) and a a cross-sectional picturepicture of of a a tissue tissue biopsy biopsy of of a a pa patienttient with with mastitis mastitis show showinging the the aL3 aL3 causing causing cuta- cuta- cross-sectional picture of a tissue biopsy of a patient with mastitis showing the aL3 causing cutaneous neous larva migrantsmigrants ((BB).). All All photos photos were were generated generated in in our our laboratory laboratory to to demonstrate demonstrate G. G. spinig- spinig- larva migrants (B). All photos were generated in our laboratory to demonstrate G. spinigenum enum aL3 morphology.morphology. aL3 morphology. 2.2. Gnathostomiasis as asas Public PublicPublic Health HealthHealth and andand Travel TravelTravel Medicine MedicineMedicine Problem ProblemProblem GnathostomiasisGnathostomiasis isisis a a parasitica parasiticparasitic disease diseasdiseas causedee causedcaused by aby by nematode a anematode nematode of the of genusof the the genus Gnathostomagenus Gna- Gna-. Severalthostoma reports.. SeveralSeveral of reportsreports the disease ofof thethe have disease disease been have have recorded b beeneen recorded inrecorded Asia and in in Asia Central Asia and and America Central Central America [6 America]. There are[6]. sporadicThereThere areare cases sporadicsporadic in non-endemic casescases in in non-endemic non-endemic countries whencountries countries travelers when when return travelers travelers home return return after home visitinghome after after the endemicvisiting thethe areas, endemicendemic especially areas,areas, Southeast espe especiallycially Asia Southeast Southeast [2,7]. G.Asia Asia spinigerum [2,7]. [2,7]. G. G. spinigerumis spinigerum the major is is speciesthe the major major causing spe- spe- humancies causing gnathostomiasis humanhuman gnathostomiasisgnathostomiasis in Southeast in in Southeast Asia, Southeast particularly Asia, Asia, particularly particularly in Thailand. in
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