Envenomation by Opisthoglyphous Snake Thamnodynastes Hypoconia (Cope, 1860) (Dipsadinae: Tachymenini) in Southern Brazil

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Toxicon 189 (2021) 1–6

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Toxicon

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Case report Envenomation by opisthoglyphous snake Thamnodynastes hypoconia (Cope, 1860) (Dipsadinae: Tachymenini) in southern Brazil

Marluci Müller Rebelato a,*, Vinícius Yuri Kingeski Ferri a, Diego Anderson Dalmolin b, Alexandro Marques Tozetti c, Laura Verrastro d a Programa de Pos-graduaç´ ao˜ em Biologia Animal, Laboratorio´ de Herpetologia, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves 9500, Agronomia, 91501-970, Porto Alegre, RS, Brazil b Programa de Pos-graduaç´ ao˜ em Biologia Animal, Laboratorio´ de Evoluçao,˜ Sistematica´ e Ecologia de Aves e Mamíferos, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves 9500, Agronomia, 91501-970, Porto Alegre, RS, Brazil c Laboratorio´ de Ecologia de Vertebrados Terrestres, Universidade do Vale do Rio dos Sinos, Avenida Unisinos 950, 93022-000, Sao˜ Leopoldo, RS, Brazil d Laboratorio´ de Herpetologia, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves 9500, Agronomia, 91501-970, Porto Alegre, RS, Brazil

ARTICLE INFO ABSTRACT

Keywords: We report here a case of human envenoming by Thamnodynastes hypoconia, a common and abundant non-front- Colubroid snakes fanged snake belonging to the subfamily Dipsadinae. The case was registered in the municipality of Tapes, Rio Non-front-fanged Grande do Sul state, Brazil, in a 27-year-old female. The snakebite was on the wrist of the left arm while handling Non-venomous snake the snake in a field outing. No pain sensation was noted during the bite, and after 20 minutes edema developed Snakebite along the hand and forearm with a slight sensation of numbness and mild pain when moving the fingers.After 15 Thamnodynastes hours, the victim began to develop erythema, paraesthesia, and a sensation of warmth at the bite site. After 30 hours, ecchymosis occurred on the fingers and forearms, and the edema began to decrease. After 70 hours from the time of the bite, ecchymosis along with pruritus and mild pain were still evident. The patient was treated with prescribed medications, and after 7 days no further symptoms were observed. This is the first reported case of envenoming by T. hypoconia.

1. Introduction has aglyphous or opisthoglyphous dentition and are considered harm less due to their inefficientvenom injection in humans (Gans and Elliott, The annual number of people bitten by snakes in Brazil can reach 1968; Weinstein and Kardong, 1994). However, Dipsadinae, called close to 30,000. In 2017, out of a total 28,000 cases, 23,000 (~81%) “non-venomous”, have the Duvernoy’s gland which is a homologous were caused by venomous snakes (Viperidae and Elapidae; front-fanged structure to the venom gland of viperids and elapids (Jackson et al., snakes, FFS), 1890 (~7%) by non-venomous snakes and 3245 by un 2017). The Duvernoy’s gland produces toxins used to subdue prey identified snakes (~12%) (SINAN, 2019). However, the number of ac (Kardong, 2002), but very little is known about these toxins and their cidents with non-venomous and non-front-fanged snakes (NFFS) snakes actions on living tissues (Ching et al, 2006, 2012; Fry et al., 2003; Pei in Brazil is likely underestimated since many bite victims do not seek choto et al, 2011, 2012). In general, the symptoms of accidents caused medical attention in a healthcare center, and as such are unreported. In by these non-venomous snakes are local pain, edema, and ecchymosis Brazil, accidents with non-venomous snakes are caused mainly by spe (Prado-Franceschi and Hyslop, 2002). cies of the family Colubridae and subfamilies Colubrinae and Dipsadi In Brazil, most accidents with Dipsadinae species occur with the nae, which are rear-fanged snakes (RFS) orNFFS (Junqueira-de-Azevedo genera Clelia, Erythrolamprus (former Liophis), Helicops, Philodryas, et al., 2016; Salomao˜ et al., 2003; Weinstein et al., 2011). Oxyrhopus, Sibynomorphus, Thamnodynastes and Xenodon (former Unlike snakes of the Viperidae and Elapidae families, which have Lystrophis) (Araújo et al., 2018; Barbosa et al., 2020; Prado-Franceschi solenoglyphous and proteroglyphous dentition, respectively, Dipsadinae and Hyslop, 2002; Quintela, 2010; Salomao˜ et al., 2003; Silveira and

* Corresponding author. E-mail addresses: [email protected], [email protected] (M.M. Rebelato), [email protected] (V.Y.K. Ferri), [email protected] (D.A. Dalmolin), [email protected] (A.M. Tozetti), [email protected] (L. Verrastro). https://doi.org/10.1016/j.toxicon.2020.10.022 Received 22 June 2020; Received in revised form 19 October 2020; Accepted 27 October 2020 Available online 2 November 2020 0041-0101/© 2020 Elsevier Ltd. All rights reserved. M.M. Rebelato et al. Toxicon 189 (2021) 1–6

Nishioka, 1992). Thamnodynastes spp. are neotropical in nature and It is important to highlight that based on the general aspects of the belong to the Tachymenini tribe (Zaher et al., 2009). Thamnodynastes hand and general symptoms, the medical team believed that it was a hypoconia (Cope, 1860) (Fig. 1) occurs in the northeast, midwest, venomous snakebite from the Bothrops genus. They recommended that southeast, and south of Brazil, Paraguay, Uruguay, and Argentina the victim be transferred to another hospital at Porto Alegre city (the (Franco, 1999; Giraudo, 2001). It is a small opisthoglyphous snake, state capital) situated 130 km from the medical center where the bite reaching approximately 70 cm in total length and displays a very was initially evaluated. The professionals reported that Porto Alegre was aggressive behavior when threatened (Giraudo, 2001). It is a viviparous, the closest urban center with the availability of antivenom for Bothrops nocturnal species, which feeds primarily on frogs (Bellini et al, 2013, bite. The victim, a professional herpetologist, declared that the snake 2014; Rebelato et al., 2016, 2020). We report a case of symptoms was not a Bothrops but Thamnodynastes hypoconia. The hospital team following the bite to a researcher during manipulation of the snake contacted the Toxicological Information Center of Rio Grande do Sul T. hypoconia in the field in southern Brazil. (Centro de Informaçao˜ Toxicologica´ - CIT), and mentioned the species involved in the accident. The CIT, which advises and guides the occur 2. Case report rence of toxic accidents in the state, confirmed that bites from T. hypoconia had no known medical risk and the patient could leave the On Feb 15th, 2016, a 27-year-old female, 68 kg body weight, 183 cm hospital. Before being discharged, the patient had the bite site cleaned tall, was bitten while handling a T. hypoconia (32.4 cm snout-vent with iodine and covered with a bandage (Fig. 3E). Paracetamol 500 mg length; 11 cm tail length and 10.30 g body weight) to take body mea and Ibuprofen 400 mg were also prescribed as analgesic and anti- surements when the snake attached its jaws to the left hand wrist inflammatory every 6 h, but the patient used only Ibuprofen. (Fig. 3A). The accident happened around 8:45 p.m. during a fieldouting On the second day, 15 hours after the accident, the hand and forearm in a wetland area on the shore of the Patos Lagoon, in the municipality of showed edema, erythema, paraesthesia, and a sense of warmth at the Tapes, Rio Grande do Sul state, Brazil (Fig. 2). bite site with mild pain (Fig. 4A). After 20 hours, body temperature ◦ The snake held its bite for approximately 60 seconds before being (37.4 C), blood pressure (130/80 mm), and heart rate (97 bpm) were manually removed, forcing the opening of the mandible by raising the measured again. On the third day, after 30 hours, all fingers and inner maxilla. The bite caused minimal immediate pain due to perforation by part of the forearm presented ecchymosis and moderate pain when the snake’s teeth, and after the snake is removed from the left wrist, two performing any muscular effort (Fig. 4B and C), however, the edema perforations were observed due to puncture by the opisthoglyphus began to decrease. On the fourth day, 70 hours after the bite, the hand dentition with slight bleeding surrounded by mild local edema (Fig. 3B). and forearm no longer showed edema and the ecchymosis changed from After 20 minutes, the edema spread over the hand and forearm, with a a purple color to a yellowish-green color, followed by pruritus, mild slight sensation of numbness and pain during fingermovement (Fig. 3C). pain, and itching (Fig. 4D and E). On the fifth day, the yellowish-green Three hours after the incident, the left hand was quite swollen in relation color was practically imperceptible and there was no more pain when to the right hand (Fig. 3D). performing any physical effort. Finally, on the seventh day no symptoms Following 4 hours of the accident, the victim was taken to the Basic were visible. It is important to remember that these symptoms happened Health Unit at Arambar´e city. The following vital signs were recorded: in a healthy woman who had no medical history of allergies, chronic or ◦ body temperature: 36.7 C, blood pressure: 110/60 mm, and heart rate: autoimmune diseases, nor use of any prescribed or other medications. 85 bpm. The medication Celestamine® (dexchlorpheniramine maleate - The victim had a history of prior bites by T. hypoconia during field ac 2 mg + betamethasone - 0.25 mg) was prescribed, with posology of one tivities without symptoms observed. However, this was the firsttime the tablet every 8 hours for 5 days. During the attendance, the health pro snake bit and held on for longer, managing to insert the opisthoglyph fessional requested the patient go to Nossa Senhora Aperecida Hospital fangs. emergency room, a more specialized health center at the municipality of Permits from the Instituto Chico Mendes de Conservaçao˜ da Bio Camaqua˜ (35 km distant), since he believed that the symptoms were diversidade (ICMBio; SISBio nº 50062-5; Ministry of Environment, Gov unusual for an accident involving a non-venomous snake. ernment of Brazil) allowed us to collect and register it in the

Fig. 1. Specimen of Thamnodynastes hypoconia, Tapes, Rio Grande do Sul, Brazil. Photo by Natalia Dallagnol Vargas.

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Fig. 2. Map showing the location where the accident occurred. The black star indicates the site on the shore of Patos Lagoon, in Tapes municipality, Rio Grande do ◦ ′ ′′ ◦ ′ ′′ Sul state, Brazil (30 52 7.15 S and 51 23 41.92 W).

Fig. 3. A) Thamnodynastes hypoconia at the bite moment.; B) Opisthoglyph dentition marks observed from the bite; C) Edema on the affected hand 20 minutes after the accident; D) Edema present 3 hours after the bite; E) Bandage on the hand after medical care.

Herpetological Collection of the Laboratory of Ecology of Terrestrial 3. Discussion Vertebrates (Laboratorio´ de Ecologia de Vertebrados Terrestres, LEVERT) of the University of Vale do Rio dos Sinos (Unisinos) under the number This is the first reported case of a snakebite accident caused by the CHLEVT330. non-front-fanged colubroid species, T. hypoconia. Although there are other records for the genus Thamnodynastes (Araújo et al., 2018; Diaz et al., 2004; Hoge, 1952; Lema, 1978; Prado-Franceschi and Hyslop, 2002; Salomao˜ et al., 2003), this is the first for this species. The other

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Fig. 4. A) Edema and erythema 15 hours after the accident; B–C) Ecchymosis on the hand and forearm after 30 hours; D-E) Ecchymosis changing from purple to yellowish-green after 70 hours. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.) case reports were with the congeneric T. pallidus, with one case in Accidents involving T. strigatus are not well documented, although northeastern Brazil (Araújo et al., 2018) and one in Venezuela (Diaz this species is associated with a large number of accidents in Brazil et al., 2004); and with the congeneric T. strigatus (Hoge, 1952). All three (Hoge, 1952; Puorto and França, 2003). A study on the venomic profile cases involved researchers who were bitten on the hand during manip of T. strigatus revealed metalloproteinases with a proteolytic activity ulation, which demonstrates a general aggressive-defensive behavior of previously identifiedin other snakes of the Colubridae family (Assakura Thamnodynastes spp. Salomao˜ et al. (2003) highlights that bites by et al., 1994; Lemoine et al., 2004). However, the function of these non-venomous snakes have been most frequently reported on the hands. proteins has not been identifiedyet (Ching et al., 2012). We emphasize The aforementioned reports on T. pallidus also cited edema, ecchy here the importance of knowing the toxin profile of non-venomous mosis, mild pain, and a sense of warmth at the bite site. In the accident snakes, given the enormous pharmacological potential that these sub recorded by Araújo et al. (2018), the symptoms were milder and ceased stances can present (Georgieva et al., 2008). An experiment with after 36 hours without using medication. In the case reported by Diaz T. strigilis venom injected in rats showed neurotoxic symptoms, edema, et al. (2004), in addition to the symptoms described above, excessive local necrosis, and both local and systemic hemorrhage (Lemoine et al., salivation with metallic taste and a severe headache was also recorded. 2004). Among Dipsadinae, the venom of Philodryas spp. deserves greater In this case, the patient was medicated with hydrocortisone and anal attention due to the large number of cases involving the genus (Medeiros gesic, and after 36 hours he no longer had evidence of edema. In the case et al., 2010) and the potential risks they represent. Of particular reported here, the edema also decreased after 30 hours of the accident, importance is the snake P. olfersii, which has been responsible for mul but the ecchymosis was still visible on the forearm after 70 hours, and tiple accidents and reported as a potential cause of death in two children after one week all observed symptoms had disappeared. The specimens (Campbell and Lamar, 2004; Salomao˜ and Di-Bernardo, 1995). of T. pallidus responsible for these accidents had a larger body size than We highlight here the lack of available information concerning the the T. hypoconia specimen involved here (10.30 g body mass, 43.4 cm of potential medical risks posed by the majority of colubroid NFFS, and the total length), which was possibly a subadult. In the accident reported by problems that arise when health professionals mistake the envenoming Diaz et al. (2004), the specimen had body mass of 25 g and 57 cm of total symptoms from colubroid NFFS bites with those of significantly length, and Araújo et al. (2018) reported a specimen with a 20 g body venomous species, mainly within the genus Bothrops (Viperidae) in mass and 54.8 cm of total length. The longer duration of the snakebite Brazil. When the victim is unable to identify the species or take the effects despite of its smaller body size suggests that the venom from specimen to the nearest health center, the false diagnosis can lead to the T. hypoconia may be more potent than the venom of T. pallidus. Lastly, as unnecessary application of antivenom causing even greater medical risk in Araújo et al. (2018) and Diaz et al. (2004) reports, we also did not to the victim (Bernarde, 2014; Menegucci et al., 2019; Silveira and observe secondary infection caused by the bite. Nishioka, 1992). This demonstrates the need to standardize care

4 M.M. Rebelato et al. Toxicon 189 (2021) 1–6 protocols for correct diagnosis and proper medical treatment for victims Bernarde, P.S., 2014. Serpentes Peçonhentas e Acidentes Ofídicos no Brasil. Anolis Books of colubroid NFFS, those with aglyphous and opisthoglyphous dentition. Editora. Campbell, J.A., Lamar, W.W., 2004. The Venomous Reptiles of the Western Hemisphere. The case reported here and other reports show that the symptoms Cornell University Press, Ithaca. following the bite of T. hypoconia resolved within a few days following Ching, A.T.C., Paes Leme, A.F., Zelanis, A., Rocha, M.M.T., Furtado, M.F.D., Silva, D.A., symptomatic treatment with analgesic and anti-inflammatory medica Trugilho, M.R.O., da Rocha, S.L.G., Perales, J., Ho, P.L., Serrano, S.M.T., Junqueira- de-Azevedo, I.L.M., 2012. Venomics profiling of Thamnodynastes strigatus unveils tions. In some cases involving Colubridae, there is no need for medica matrix metalloproteinases and other novel proteins recruited to the toxin arsenal of tion, just the application of ice to reduce edema, resting and observation rear-fanged snakes. J. Proteome Res. 11, 1152–1162. https://doi.org/10.1021/ (Puorto and França, 2003). Our case report reinforces that researchers pr200876c. Ching, A.T.C., Rocha, M.M.T., Paes Leme, A.F., Pimenta, D.C., Furtado, M.F.D., must take precautions when handling snakes belonging to Colubridae Serrano, S.M.T., Ho, P.L., Junqueira-de-Azevedo, I.L.M., 2006. Some aspects of the family and Dipsadinae subfamily (Menegucci et al., 2019). We show that venom proteome of the Colubridae snake Philodryas olfersii revealed from a T. hypoconia, a snake species considered non-venomous, should be Duvernoy’s (venom) gland transcriptome. FEBS Lett. 580, 4417–4422. https://doi. org/10.1016/j.febslet.2006.07.010. handled with care based on the envenoming symptoms observed in this Diaz, F., Navarrete, L.F., Pefaur, J., Rodriguez-Acosta, A., 2004. Envenomation by case. We believe that snakes classified as non-venomous should be neotropical opistoglyphous colubrid Thamnodynastes cf. pallidus Linné, 1758 reviewed and not treated negligently. (serpentes:colubridae) in Venezuela. Rev. Inst. Med. Trop. Sao Paulo 46, 287–290. It is important to mention that the person involved in the case pre https://doi.org/10.1590/S0036-46652004000500011. Franco, F.L., 1999. Relaçoes˜ filogeneticas´ entre os gêneros da tribo Tachymenini Bailey sented here had a prior history of having been bitten by the same species (1967) (Serpentes; Colubridae). Ph.D. Dissertation, Universidade de Sao˜ Paulo, at previous times during manipulation in field activities. However, this Brazil. was the firsttime that the snake opened its mouth completely managing Fry, B.G., Lumsden, N.G., Wüster, W., Wickramaratna, J.C., Hodgson, W.C., Manjunatha Kini, R., 2003. Isolation of a neurotoxin (α-colubritoxin) from a nonvenomous to insert the opisthoglyph fangs, causing perforation of the skin and Colubrid: evidence for early origin of venom in snakes. J. Mol. Evol. 57, 446–452. venom injection. Thus, the symptoms in the case reported here appeared https://doi.org/10.1007/s00239-003-2497-3. to be due to venom-induced effects and not a localized allergic reaction Gans, C., Elliott, W.B., 1968. Snake venoms: production, injection, action. Adv. Oral Biol. 3, 45–81. https://doi.org/10.1016/B978-1-4832-3119-8.50009-3. to salivary secretions. Reinforcing this interpretation, the victim when Georgieva, D., Arni, R.K., Betzel, C., 2008. 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Menegucci, R.C., Bernarde, P.S., Monteiro, W.M., Bisneto, P.F., Martins, M., 2019. Acknowledgements Envenomation by an opisthoglyphous snake, Erythrolamprus aesculapii (Dipsadidae), in southeastern Brazil. Rev. Soc. Bras. Med. Trop. 52, 1–3. https://doi.org/10.1590/ 0037-8682-0055-2019. We are grateful to members the fieldcrew and also to Lara de Souza Peichoto, M.E., Tavares, F.L., Santoro, M.L., MacKessy, S.P., 2012. Venom proteomes of for producing the map. M.M Rebelato was supported by a doctoral South and North American opisthoglyphous (Colubridae and Dipsadidae) snake species: a preliminary approach to understanding their biological roles. Comp. scholarship from Conselho Nacional de Desenvolvimento Científico e – ´ Biochem. Physiol. Genom. Proteonomics 7, 361 369. https://doi.org/10.1016/j. Tecnologico – Brazil (CNPq) – 141493/2015-1. We also thank the cbd.2012.08.001. 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