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Venom Ophthalmia and Ocular Complications Caused by Snake Venom

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Venom Ophthalmia and Ocular Complications Caused by Snake Venom toxins Review Venom Ophthalmia and Ocular Complications Caused by Snake Venom Kun-Che Chang 1,2 , Yu-Kai Huang 3,4,5, Yen-Wen Chen 6,7, Min-Hui Chen 8, Anthony T. Tu 9 and Yen-Chia Chen 10,11,12,* 1 Spencer Center for Vision Research, Byers Eye Institute, School of Medicine, Stanford University, Palo Alto, CA 94304, USA; [email protected] 2 Department of Ophthalmology, Louis J. Fox Center for Vision Restoration, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA 3 Graduate Institute of Clinical Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung 80708, Taiwan; [email protected] 4 Division of Neurosurgery, Department of Surgery, Kaohsiung Medical University Hospital, Kaohsiung 80708, Taiwan 5 Department of Surgery, Kaohsiung Municipal Ta-Tung Hospital, Kaohsiung 80145, Taiwan 6 Department of Chest Medicine, Taipei Veterans General Hospital, Taipei 11217, Taiwan; [email protected] 7 Institute of Clinical Medicine, National Yang-Ming University, Taipei 11221, Taiwan 8 Enkang Clinic, New Taipei 23144, Taiwan; [email protected] 9 Department of Biochemistry and Molecular Biology, Colorado State University, Ft. Collins, CO 80523, USA; [email protected] 10 Emergency Department, Taipei Veterans General Hospital, Taipei 11217, Taiwan 11 Department of Emergency Medicine, School of Medicine, National Yang-Ming University, Taipei 11221, Taiwan 12 National Defense Medical Center, Taipei 11490, Taiwan * Correspondence: [email protected] Received: 12 August 2020; Accepted: 3 September 2020; Published: 8 September 2020 Abstract: Little is known about the detailed clinical description, pathophysiology, and efficacy of treatments for ocular envenoming (venom ophthalmia) caused by venom of the spitting elapid and other snakes, as well as ocular complications caused by snake venom injection. In this paper, we review clinical information of case reports regarding venom ophthalmia and snake venom injection with associated ocular injuries in Asia, Africa, and the United States. We also review the literature of snake venom such as their compositions, properties, and toxic effects. Based on the available clinical information and animal studies, we further discuss possible mechanisms of venom ophthalmia derived from two different routes (Duvernoy’s gland in the mouth and nuchal gland in the dorsal neck) and the pathophysiology of snake venom injection induced ocular complications, including corneal edema, corneal erosion, cataract, ocular inflammation, retinal hemorrhage, acute angle closure glaucoma, as well as ptosis, diplopia, and photophobia. Finally, we discuss the appropriate first aid and novel strategies for treating venom ophthalmia and snake envenoming. Keywords: snake venom; snakebite; spitting venom; nuchal gland; corneal edema; retinal hemorrhage Key Contribution: This review article focuses on venom ophthalmia derived from two different routes (Duvernoy’s gland in the mouth and nuchal gland in the dorsal neck) and the pathophysiology of snake venom injection induced ocular complications, and then uncovers the possible underlying mechanisms. Toxins 2020, 12, 576; doi:10.3390/toxins12090576 www.mdpi.com/journal/toxins Toxins 2020, 12, x FOR PEER REVIEW 2 of 17 Keywords: snake venom; snakebite; spitting venom; nuchal gland; corneal edema; retinal hemorrhage Key Contribution: This review article focuses on venom ophthalmia derived from two different routes (Duvernoy’s gland in the mouth and nuchal gland in the dorsal neck) and the pathophysiology of snake venom injection induced ocular complications, and then uncovers the possible underlying mechanisms. Toxins 2020 12 1. Introduction, , 576 2 of 15 Snakes are carnivorous reptiles, which are cold-blooded animals. They inhabit every continent and1. Introductionocean (sea snake) [1] except Antarctica. Some snakes are venomous while some are not. VenomousSnakes snakes are carnivorous comprise reptiles, four whichfamilies, are cold-bloodedincluding Colubridae animals., TheyElapidae inhabit, Viperidae every continent, and Atractaspididaeand ocean (sea [2]. snake) In this [1] except review, Antarctica. we distinguish Some snakes between are venomousvenom-induced while some ophthalmias, are not. Venomous venom spraysnakes (Figure comprise 1A), fourand venom families, injection including (FigureColubridae 1B). We, Elapidae further, Viperidae discuss ,two and sourcesAtractaspididae of venom[2]. spray, In this initiatingreview, wefrom distinguish the modified between salivary venom-induced gland (Duvernoy’s ophthalmias, glands, venom Figure spray 2A) (Figureor prey-derived1A), and venomtoxin storageinjection glands (Figure (nuchal1B). We gland, further Figu discussre 2B). twoAmong sources snake of venomspecies, spray,spitting initiating cobras, froma member the modified of the Elapidaesalivary family gland snakes, (Duvernoy’s can spit glands, venom Figure from2 A)Duvernoy’s or prey-derived gland toxinwhile storageirritated glands or threatened. (nuchal gland, The tigerFigure keelback,2B). Among a member snake of species, the Colubridae spitting family cobras, snakes a member often offound the Elapidaein East Asia,family conducts snakes, a can toxin spit sprayvenom from from its Duvernoy’snuchal gland. gland After while a toxin irritated spray or attack, threatened. the eyes The are tiger most keelback, often affected, a member causing of the inflammatoryColubridae family responses snakes in oftenthe anterior found in segment East Asia, of the conducts eye. In a toxinvenom spray spray from ophthalmia, its nuchal many gland. symptomsAfter a toxin such spray as hyperemia, attack, the uveitis, eyes are and most corn ofteneal erosions affected, are causing common inflammatory complications responses after venom in the sprayanterior [3]. segment of the eye. In venom spray ophthalmia, many symptoms such as hyperemia, uveitis, and corneal erosions are common complications after venom spray [3]. Toxins 2020, 12, x FOR PEER REVIEW 3 of 17 Figure 1. Snake venom ophthalmia via venom spray (A) and venom injection (B). Figure 1. Snake venom ophthalmia via venom spray (A) and venom injection (B). Figure 2. Duvernoy’s gland (A) and nuchal gland (B) are two different systems of venom spray. Figure 2. Duvernoy’s gland (A) and nuchal gland (B) are two different systems of venom spray. Ocular complications in the posterior segment are often observed after snakebite. An epidemiological Ocular complications in the posterior segment are often observed after snakebite. An study of 180 snakebite patients in India reported that 69% of victims present with ocular neuroparalytic epidemiological study of 180 snakebite patients in India reported that 69% of victims present with manifestations [4]. Most viperide snakes discharge venom as the fangs hook into the victim, and then ocular neuroparalytic manifestations [4]. Most viperide snakes discharge venom as the fangs hook immediately release the bite. However, some species (e.g., Lachesis) may hold the bite, discharging a into the victim, and then immediately release the bite. However, some species (e.g., Lachesis) may larger amount of venom to kill the victim, especially in times of starvation. So far, about 59 protein hold the bite, discharging a larger amount of venom to kill the victim, especially in times of familiesstarvation. have been So identifiedfar, about in59 venoms,protein families which arehave capable been identified of inflicting in venoms, neurotoxicity, which are cytotoxicity, capable of hemotoxicity,inflicting and neurotoxicity, myotoxicity, cytotoxicity, [5] and most hemotoxici snake venomsty, and have myotoxicity, mixed eff [5]ects. and Hemotoxins most snake in venoms snake venomhave cause mixed hemolysis, effects. destruction Hemotoxins of in erythrocytes, snake venom and ca blooduse hemolysis, clotting. Sincedestruction hemotoxins of erythrocytes, are abundant and blood clotting. Since hemotoxins are abundant in viperidae, ocular hemorrhage and secondary inflammatory responses are the most common ocular complications by viper snake envenoming. Neurotoxins in snake venom cause neurological disorders in the eye, such as ocular muscle paralysis, ptosis, and diplopia. Without immediate treatment, patients can be left with permanent tissue damage, blindness, or even death from respiratory muscle paralysis. In this review, we focus on venomous neurotoxins and hemotoxins and the possible ocular pathophysiology after venom spray or venom injection. We also discuss the current development of therapeutic strategies for treating venom-induced ocular complications. 2. Snake Venom/Toxin Cause Ocular Complications 2.1. Spitting Venom and Sprayed Toxin 2.1.1. Venom Spat from Duvernoy’s Gland Naja is a genus of venomous elapidae, also known as cobras. Several species of Naja cobras can spit their venom from Duvernoy’s gland (Figure 2A), where venom is generated and stored, through fangs onto victims. The cobras can spit venom onto targets about 1.5 m away [6]. To understand the cobras’ spitting behavior, a study utilized photos of human faces or hands to trigger spitting of two cobras, Naja nigricollis and N. pallida [7]. That study revealed that most cobras only respond to moving faces but not to hands within 10 s (79% of N. nigricollis and 67% of N. pallida). Spitting patterns on the photos showed that the venom streamlines are either between the eyes or at one eye, suggesting the intent to hit at least one eye of an aggressor. Another group investigated target tracking during cobra venom spitting [8]. They observed that cobras perform
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