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The Bold and the Beautiful: a Neurotoxicity Comparison of New World Coral Snakes in the Micruroides and Micrurus Genera and Relative Neutralization by Antivenom

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The Bold and the Beautiful: a Neurotoxicity Comparison of New World Coral Snakes in the Micruroides and Micrurus Genera and Relative Neutralization by Antivenom Neurotox Res DOI 10.1007/s12640-017-9771-4 ORIGINAL ARTICLE The Bold and the Beautiful: a Neurotoxicity Comparison of New World Coral Snakes in the Micruroides and Micrurus Genera and Relative Neutralization by Antivenom Daryl C. Yang1 & James Dobson2 & Chip Cochran3 & Daniel Dashevsky2 & Kevin Arbuckle4 & Melisa Benard5 & Leslie Boyer6 & Alejandro Alagón5 & Iwan Hendrikx1 & Wayne C. Hodgson1 & Bryan G. Fry2 Received: 9 March 2017 /Revised: 29 May 2017 /Accepted: 13 June 2017 # Springer Science+Business Media, LLC 2017 Abstract Coral snake envenomations are well characterized envenomations in the USA as well as additional species from to be lethally neurotoxic. Despite this, few multispecies, neu- the Americas. The use of Coralmyn® coral snake antivenom rotoxicity and antivenom efficacy comparisons have been un- was effective in neutralizing the neurotoxic effects exhibited dertaken and only for the Micrurus genus; Micruroides has by the venom of M. fulvius but was ineffective against the remained entirely uninvestigated. As the USA’s supplier of venoms of Micrurus tener, Micrurus spixii, Micrurus antivenom has currently stopped production, alternative pyrrhocryptus,andMicruroides euryxanthus. Our results sug- sources need to be explored. The Mexican manufacturer gest that the Mexican antivenom may be clinically useful for Bioclon uses species genetically related to USA species, thus the treatment of M. fulvius in the USA but may be of only we investigated the efficacy against Micrurus fulvius (eastern limited efficacy against the other species studied. coral snake), the main species responsible for lethal Keywords Venom . Neurotoxicity . Antivenom . Micrurus . Daryl C. Yang, James Dobson, and Chip Cochran contributed equally to . this work. Micruroides Coral snake Electronic supplementary material The online version of this article (doi:10.1007/s12640-017-9771-4) contains supplementary material, which is available to authorized users. Introduction * Wayne C. Hodgson The New World coral snakes consist of three genera: [email protected] Leptomicrurus (five species), Micruroides (one species), and * Bryan G. Fry Micrurus (approx. 70 species) (Roze 1996). The two less [email protected] speciose genera are restricted in their geographic range; Leptomicrurus is only found in close proximity to the 1 Monash Venom Group, Monash University, Clayton, VIC 3800, Australia Amazon basin (Campbell and Lamar 1989)while Micruroides is restricted in the United States to the southern 2 Venom Evolution Lab, School of Biological Sciences, University of Queensland, St Lucia, QLD 4072, Australia half of Arizona and extreme southeastern New Mexico, south into the northwestern Mexican states of Sonora, extreme south- 3 Department of Earth and Biological Sciences, Loma Linda University, Loma Linda, CA 92350, USA western Chihuahua, and Sinaloa, with an insular population occurring on Isla Tiburón (Campbell and Lamar 2004). In con- 4 Department of Biosciences, College of Science, Swansea University, Swansea SA2 8PP, UK trast, snakes of the genus Micrurus distribution ranges from the southeastern USA to Argentina (Jorge da Silva and Sites 2001). 5 Instituto de Biotecnología, Universidad Nacional Autónoma de México, Av. Universidad # 2001, 62210 Cuernavaca, Morelos, Bites from most of these snakes, with the exception of the Mexico very small Micruroides, are considered potentially life- 6 Venom Immunochemistry, Pharmacology and Emergency Response threatening due to deaths reported from species across their (VIPER) Institute, University of Arizona College of Medicine, geographical range (Bucaretchi et al. 2016; Manock et al. Tucson, AZ, USA 2008;Morganetal.2007). The venom is considered to be Neurotox Res primarily neurotoxic, and the most common cause of death is snake antivenom (NACSA; Wyeth, United States) and paralysis-induced hypoxia (Vital-Brazil 1987) highlighting Coralmyn® coral snake antivenom (Bioclon, Mexico), in order the importance for each country that contains coral snakes in to ascertain their ability to neutralize the lethal components in having access to antivenoms capable of neutralizing the neu- both M. fulvius and M. tener, two American coral snake species. rotoxic effects of coral snake envenomation. Currently, the While the use of Coralmyn® was effective in neutralizing the most effective treatment for coral snake envenomations is LD50 doses of both M. fulvius and M. tener venoms, the use of the administration of specific antivenom coupled with direct NACSAwasineffectiveinneutralizingthelethalityof threevary- treatment of symptoms such as pre-synaptic neurotoxicity not ing doses of venom from M. tener. In South America, a study by neutralized by antivenom (Peterson 2006). As antivenoms are Camargo et al. (2011) investigated the efficacy of coral snake produced by inoculating livestock (generally sheep or horses) antivenom against the venom of Micrurus pyrrhocryptus.It against venom from a particular species or selection of species was shown that both the commercial coral snake antivenom and purifying the resulting antibodies (Angulo et al. 1997; (Instituto Butantan, Brazil) and the specific antivenom raised Rojas et al. 1994), antivenoms can be partially or wholly in- against the venom of M. pyrrhocryptus were effective in neutral- effective against the venom from species not included in pro- izing its neurotoxic effects. However, it remained to be seen duction (Tanaka et al. 2010; Boyer et al. 2015). Nonetheless, whether Coralmyn® coral snake antivenom, which was raised experimental (Bolanos et al. 1975; Silva et al. 2016) as well as against Micrurus nigrocinctus nigrocinctus (black-banded coral clinical evidence of cross-neutralization has been reported snake) venom, would be effective against M. pyrrhocryptus ven- even for non-related snake species (Isbister et al. 2014). om. Moreover, as the use of Coralmyn® was effective against the The reason antivenoms sometimes fail when treating bites venoms of M. fulvius and M. tener in a murine model, it was from coral snake species, whose venom was not included in hypothesized that the antivenom would be equally as effective the production of antivenom, has recently become more sa- in an in vitro preparation. The current study is of clinical signif- lient as studies have revealed that the variation in coral snake icance as the production of NACSAwas discontinued by Wyeth venoms is deeper and more widespread than previously in 2008 (Wood et al. 2013) and, thus, it is imperative that the presumed. In particular, Aird and Jorge da Silva (1991)pro- efficacy of other coral snake antivenom is determined. vided evidence based on enzymatic activities that some coral Historically, murine LD50 studies have been performed in snake venoms more closely resemble the venoms of more order to determine relative neurotoxicity of venoms (WHO distantly related snakes such as Bungarus, Bothrops,orNaja 2010). In some circumstances, however, these can be supple- than other coral snakes. Proteomic and transcriptomic analy- mented by in vitro studies such as that of the chick biventer ses of coral snakes from across the Americas indicate that, cervicis nerve-muscle preparation (Hodgson and broadly speaking, some coral snake venoms contain three- Wickramaratna 2002). Using this preparation, the neurotoxicity finger toxins (3FTx) as their most abundant components while of venoms can be examined by observing the time in which the others are composed primarily of phospholipase A2 (PLA2) venom/toxins produces 90% inhibition of nerve-mediated (Fernandez et al. 2015; Rey-Suarez et al. 2016, Vergara et al. twitches (t90 values). However, there may be extreme variation 2014; Lomonte et al. 2016a). between the synapsid (mouse) and diapsid (bird) results if the There are currently four antivenoms primarily used in the venoms are evolutionarily shaped to be taxon-specific (Fry et al. treatment of New World coral snake bites (Table 1). The pro- 2003; Heyborne and Mackessy 2013; Lumsden et al. 2004a, b, duction of North American coral snake antivenom (NACSA) Lumsden et al. 2005a; Utkin et al. 2015). Such specificity has was halted in 2008, and remaining stocks have diminished been described in vivo for the venoms of M. pyrrhocryptus and while repeatedly having their effectiveness tested and expiry M. spixii (Jorge da Silva and Aird 2001). There, they determined dates extended (Wood et al. 2013); a single lot was released in LD50 values of whole venoms on prey and non-prey models and 2016 for limited distribution in the USA (Supplementary File showed that they are, respectively, six and two times more lethal 1). The general shortage of coral snake antivenom in the USA to the snake Lyophis typhlus than to mice. The case of M. tener, has led to the proposal that the Mexican Coralmyn® coral on the other hand, appears to be somewhat different because, snake antivenom (Bioclon, Mexico) be used in its place. even though a few apparently snake specific toxins have been Due to the diversity of coral snakes in each country where isolated from it, the whole venom has no proven specificity they are found being greater than the diversity used in produc- towardssnakes(Bénard-Valleetal.2014). tion, testing the cross reactivity of antivenom on species that Chick biventer assays are sometimes utilized in predicting were not part of its manufacture remains medically important. clinical efficacy of antivenoms; however, chick biventer assays The use of commercially available coral snake antivenoms is are not an antivenom challenge as
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