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A case report of human intoxication due to a snakebite by the opisthoglyphous dipsadid Thamnodynastes lanei Bailey, Thomas & Silva-Jr, 2005

Abstract

We present a case of human intoxication due to a snakebite by the opisthoglyphous dipsadid Thamnodynastes lanei. A 26-year-old man was bitten on the right hand and was not medicated. Bleeding lasted a few seconds, while paresthesia, chills, and headache persisted for up to 10 hours. The pain disappeared after a week, and the edema, itching, and prickling persisted for another 3 days. Although this patient’s symptoms were typical of bites by South American opisthoglyphous snakes, they persisted longer than those of bites by some congeneric species. Our report adds a species to the list of medically relevant snakes.

Keywords:
Amazonia; Public health; Tropical disease

INTRODUCTION

Snakebite has been considered a priority neglected tropical disease by the World Health Organization, since the incidence and severity are high enough to generate a demand for specific public health policies11. Chippaux JP. Snakebite envenomation turns again into a neglected tropical disease! J Venom Anim Toxins. 2017;23:38.. Snakebites are also a matter of social interest since most patients are poor people who live and work in rural areas11. Chippaux JP. Snakebite envenomation turns again into a neglected tropical disease! J Venom Anim Toxins. 2017;23:38.. The first step towards effective public health policies is to determine the list of snakes that health professionals should be familiar with for identifying species and bite symptoms. However, this may not be a straightforward task when considering opisthoglyphous snakes because there is a debate about their classification in relation to public health, since symptoms caused by the bites of these snakes vary widely among species and patients33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58..

Opisthoglyphous snakes have traditionally been classified as non-venomous snakes and are considered to be harmless to humans22. Weinstein SA, Warrell DA, White J, Keyler DE. “Venomous” Bites from Non-Venomous Snakes: A Critical Analysis of Risk and Management of “Colubrid”. 1da ed. London: Elsevier; 2011. 336 p.. However, some species of the Colubridae and Dipsadidae families may cause local (e.g., bleeding and swelling) and systemic symptoms (e.g., fever and sweating), and even death, although a few cases are anecdotal22. Weinstein SA, Warrell DA, White J, Keyler DE. “Venomous” Bites from Non-Venomous Snakes: A Critical Analysis of Risk and Management of “Colubrid”. 1da ed. London: Elsevier; 2011. 336 p.. Although biochemical and epidemiological studies on South American pitvipers (e.g., Crotalus and Bothrops) are relatively common, the potential toxicity of Colubridae and Dipsadidae families is poorly known33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.,44. Ching A, Paes Leme AF, Zelanis A, Rocha MM, Furtado MdeF, Silva DA, et al. Venomics profling of Thamnodynastes strigatus unveils matrix metalloproteinases and other novel proteins recruited to the toxin arsenal of rear-fanged snakes. J Proteome Res. 2012;11(2):1152-62.. Therefore, it can be assumed that snakebite incidence and severity of the opisthoglyphous species have been underestimated and cases studies are important for refining public health policies33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.,55. Weinstein SA, White J, Keyler DE, Warrell DA. Non-front-fanged colubroid snakes: a current evidence-based analysis of medical significance. Toxicon. 2013;69(2):103-13..

Among the South American opisthoglyphous snakes, the genus Thamnodynastes is relevant to public health. The bites of species within this genus may cause bleeding, local pain, and edema, although symptoms tend to disappear within 3-8 days33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.,66. Diaz F, Navarrete LF, Pefaur J, Rodrigues-Acosta A. Envenomation by neotropical opistoglyphous colubrid Thamnodynastes cf. pallidus Linneé, 1758 (Serpentes: Colubridae) in Venezuela. Rev Inst Med Trop São Paulo. 2004;46(5):287-90.,77. Araújo PF, Silva WM, França RC, França FGR. A case of envenomation by neotropical Ophisthoglyphous snake Thamnodynastes pallidus (Linnaeus, 1958) (Colubridae: Dipsadinae: Tachymenini) in Brazil. Rev Inst Med Trop São Paulo . 2018;38:1-4.. Several of the Thamnodynastes species share general characteristics such as beige color, slender body, long tail, short head, large eyes, and elliptical pupils88. Bailey JR, Thomas RA, Silva-Jr NJ. A revision of the South American snake genus Thamnodynastes Wagler, 1830 (Serpentes, Colubridae, Tachymenini). I. Two new species of Thamnodynastes from Central Brazil and adjacent areas, with a redefinition of and neotype designation for Thamnodynastes pallidus (Linnaeus, 1758). Phyllomedusa. 2005;4:83-101.. Therefore, differentiating species may not be a straightforward task, especially for health professionals unfamiliar with taxonomy. This is particularly critical for snakebite epidemiology because symptoms may vary among species, patients, or even among regions within a species geographic range99. Fry BG, Winkel KD, Wickramaratna JC, Hodgson WC, Wüster W. Effectiveness of snake antivenom: species and regional variation and its clinical impact. Journal of Toxicology. Toxin Rev . 2003;22(1):23-34.. Even though symptoms are usually mild, medical reports are likely to be biased by species misidentification99. Fry BG, Winkel KD, Wickramaratna JC, Hodgson WC, Wüster W. Effectiveness of snake antivenom: species and regional variation and its clinical impact. Journal of Toxicology. Toxin Rev . 2003;22(1):23-34.,1010. Bolon I, Durso AM, Botero Mesa S, Ray N, Alcoba G, Chappuis F, et al. Identifying the snake: First scoping review on practices of communities and healthcare providers confronted with snakebite across the world. PLoS ONE. 2020;15(3): e0229989.. It is not uncommon for healthcare professionals to misidentify Dipsadidae and Colubridae snakes as pitvipers33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.. Therefore, it is possible that there are unreported cases of Thamnodynastes bites that have caused more severe symptoms than those reported in the literature. Additionally, a combination of relatively severe symptoms of bites by opisthoglyphous snakes such as Thamnodynastes and misidentification of Dipsadidae and Colubridae species as pitvipers may lead to unnecessary antivenom-based treatment.

Although snakebite case studies involving Thamnodynastes have been published33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.,66. Diaz F, Navarrete LF, Pefaur J, Rodrigues-Acosta A. Envenomation by neotropical opistoglyphous colubrid Thamnodynastes cf. pallidus Linneé, 1758 (Serpentes: Colubridae) in Venezuela. Rev Inst Med Trop São Paulo. 2004;46(5):287-90.,77. Araújo PF, Silva WM, França RC, França FGR. A case of envenomation by neotropical Ophisthoglyphous snake Thamnodynastes pallidus (Linnaeus, 1958) (Colubridae: Dipsadinae: Tachymenini) in Brazil. Rev Inst Med Trop São Paulo . 2018;38:1-4., some species within this genus are still completely unknown in relation to the potential toxicity. Here, we report the symptoms of a bite by Thamnodynastes lanei, which occupies the grassy vegetation often associated to aquatic ecosystems in Argentina, Bolivia, Paraguay, and Brazilian Amazonia, Pantanal, and western Cerrado88. Bailey JR, Thomas RA, Silva-Jr NJ. A revision of the South American snake genus Thamnodynastes Wagler, 1830 (Serpentes, Colubridae, Tachymenini). I. Two new species of Thamnodynastes from Central Brazil and adjacent areas, with a redefinition of and neotype designation for Thamnodynastes pallidus (Linnaeus, 1758). Phyllomedusa. 2005;4:83-101.. We focused on providing a chronological report of symptoms, with the main objective of informing health professionals and the general population about the toxic potential of this snake.

CASE REPORT

A 26-year-old man (75 kg, 1.82 m) was bitten on the dorsal side of his right hand by an adult T. lanei (unsexed; snout-vent length, 380.7 mm; tail length, 130.9 mm; mass, 22 g; Figure 1). The snakebite occurred in a floodplain lake in the Municipality of Santarém, Pará, Brazil (2°30'42.02" S; 54°34'36.86" W; Figure 2), on April 18, 2019, at 9:46 pm. The patient is a herpetologist (senior author), who was bitten during data collection for a study on the ecology of reptile and amphibian assemblages occupying aquatic macrophyte banks. The contact of the rear fangs with the patient’s hand lasted about 40 seconds, which suggests aggressive behavior. We identified the species based on the diagnostic characters proposed in the original description of the species88. Bailey JR, Thomas RA, Silva-Jr NJ. A revision of the South American snake genus Thamnodynastes Wagler, 1830 (Serpentes, Colubridae, Tachymenini). I. Two new species of Thamnodynastes from Central Brazil and adjacent areas, with a redefinition of and neotype designation for Thamnodynastes pallidus (Linnaeus, 1758). Phyllomedusa. 2005;4:83-101.. The specimen collected was deposited in the herpetological collection of the Universidade Federal do Oeste do Pará (UFOPA), Santarém, Brazil (voucher code UFOPA-H 2096). Our specimen collection protocols were authorized by IBAMA/ICMBio/SISBIO, process nº 24072-1, and the Ethics Committee of UFOPA (process Nº 1120180049).

FIGURE 1:
Unsexed adult Thamnodynastes lanei from a floodplain lake in western Pará, Brazil. (A) Details of the head, (B) flat-neck defensive posture, and (C) general view of body shape and color. Photos by Francesca Nicole Angiolani Larrea.

FIGURE 2:
Santarém region (western Pará, Brazil). The yellow star denotes the location where the snakebite by Thamnodynastes lanei was reported.

The first symptoms (0-10 seconds) were local swelling, mild pain, and bleeding (Figure 3). The next 7 minutes were marked by moderate pain, swelling, paresthesia, itching, prickling and burning sensations. Those symptoms became severe in the next 15 minutes and were followed by edema, headache, and chills. The edema spread to the entire dorsal side of the hand and the index finger in 50 minutes, and all fingers and wrist in 4 hours. At that point, the local pain decreased, and the headache and chills disappeared. After 10 hours since the bite, the edema reduced to intense pain, and paresthesia and prickling persisted only during muscle activity. The pain completely disappeared after a week, and the swelling, itching, and prickling persisted for another 3 days. We conclude that in the absence of medication and just washing the wound with soap and water, the symptoms of T. lanei bite can persist for up to 10 days.

FIGURE 3:
Chronological evolution of Thamnodynastes lanei snakebite symptoms. (A) 10 seconds, (B) 5 minutes, (C) 40 minutes, (D) 50 minutes, and (E) 2 hours and 30 minutes after the bite.

DISCUSSION

The symptoms that we report were qualitatively expected for intoxication by Dipsadidae snakebite33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.. However, the persistence time of the symptoms was more than three times longer than that in most reported cases of Thamnodynastes bite 33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.,66. Diaz F, Navarrete LF, Pefaur J, Rodrigues-Acosta A. Envenomation by neotropical opistoglyphous colubrid Thamnodynastes cf. pallidus Linneé, 1758 (Serpentes: Colubridae) in Venezuela. Rev Inst Med Trop São Paulo. 2004;46(5):287-90.,77. Araújo PF, Silva WM, França RC, França FGR. A case of envenomation by neotropical Ophisthoglyphous snake Thamnodynastes pallidus (Linnaeus, 1958) (Colubridae: Dipsadinae: Tachymenini) in Brazil. Rev Inst Med Trop São Paulo . 2018;38:1-4.. In the literature, a case of single bite by a Thamnodynastes species has been characterized by symptoms persisting for 8 days, but most similar patients did not show symptoms for more than 3 days33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.,66. Diaz F, Navarrete LF, Pefaur J, Rodrigues-Acosta A. Envenomation by neotropical opistoglyphous colubrid Thamnodynastes cf. pallidus Linneé, 1758 (Serpentes: Colubridae) in Venezuela. Rev Inst Med Trop São Paulo. 2004;46(5):287-90.,77. Araújo PF, Silva WM, França RC, França FGR. A case of envenomation by neotropical Ophisthoglyphous snake Thamnodynastes pallidus (Linnaeus, 1958) (Colubridae: Dipsadinae: Tachymenini) in Brazil. Rev Inst Med Trop São Paulo . 2018;38:1-4.. Additionally, the edema caused by T. lanei bite is visually larger than those caused by congeneric species66. Diaz F, Navarrete LF, Pefaur J, Rodrigues-Acosta A. Envenomation by neotropical opistoglyphous colubrid Thamnodynastes cf. pallidus Linneé, 1758 (Serpentes: Colubridae) in Venezuela. Rev Inst Med Trop São Paulo. 2004;46(5):287-90.,77. Araújo PF, Silva WM, França RC, França FGR. A case of envenomation by neotropical Ophisthoglyphous snake Thamnodynastes pallidus (Linnaeus, 1958) (Colubridae: Dipsadinae: Tachymenini) in Brazil. Rev Inst Med Trop São Paulo . 2018;38:1-4.. These findings suggest interspecific variations in the biochemical structure of the Thamnodynastes venom, although immune responses are expected to vary among patients or geographic regions99. Fry BG, Winkel KD, Wickramaratna JC, Hodgson WC, Wüster W. Effectiveness of snake antivenom: species and regional variation and its clinical impact. Journal of Toxicology. Toxin Rev . 2003;22(1):23-34.. Therefore, the list of opisthoglyphous snakes that are relevant for public health (because they cause severe symptoms or are confused with pitvipers) should be constructed at species level. This highlights the relevance of timely cases studies, and the relevance of accurate taxonomic identification in reporting snakebites.

Although we found unique immune responses among reported cases of Thamnodynastes bites, we cannot quantify the effects on symptoms of unmeasured variables, such as the amount of injected venom and the patient's physical condition1111. Feitosa ES, Sampario V, Sachett J, Castro DB, Noronha MDN, Lozano JLL, et al. Snakebites as a largely neglected problem in the Brazilian Amazon: highlights of the epidemiological trends in the State of Amazonas. Rev Soc Bras Med Trop. 2015;48(Supl. 1):34-41.. However, we argue that the severity and persistence of the symptoms reported here are high enough for T. lanei to be considered a medically relevant species. Even if the most severe symptoms are mild for most people, a combination of bleeding, pain, and edema could easily lead an inexperienced health professional to identify the case as a pitviper bite33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.. This would lead to waste of antivenom, which is a traditionally scarce product in rural South America, where it is most needed. Further, unnecessary antivenom-based treatment could put patients at risk of allergenic responses and anaphylactic shock33. Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.. Ultimately, the symptoms reported here should be part of a general guide for identifying bites by opisthoglyphous snakes, which would be used for both, monitoring the toxic potential of these snakes and for avoiding unnecessary antivenom-based treatment.

Snakebite is considered a priority neglected tropical disease by the World Health Organization (WHO) and a public health concern in South America1212. Cupo P. Bites and stings from venomous animals: a neglected Brazilian tropical disease. Rev Soc Bras Med Trop . 2015;48(6):639-41.. The epidemiology of snakebites is particularly underdeveloped in Amazonia, where the incidence is relatively high and underreported1111. Feitosa ES, Sampario V, Sachett J, Castro DB, Noronha MDN, Lozano JLL, et al. Snakebites as a largely neglected problem in the Brazilian Amazon: highlights of the epidemiological trends in the State of Amazonas. Rev Soc Bras Med Trop. 2015;48(Supl. 1):34-41., and large distances to urban centers can make the search for hospitals highly costly in terms of travel time and fuel costs. While part of the rural population tends to prefer traditional medicine to hospital admission1111. Feitosa ES, Sampario V, Sachett J, Castro DB, Noronha MDN, Lozano JLL, et al. Snakebites as a largely neglected problem in the Brazilian Amazon: highlights of the epidemiological trends in the State of Amazonas. Rev Soc Bras Med Trop. 2015;48(Supl. 1):34-41., many people may decide to travel unnecessarily to treat a bite from a T. lanei snake, as the symptoms can be confused with severe cases of pitviper envenomation. Therefore, this report is relevant from clinical and epidemiological points of view as well as educational.

ACKNOWLEDGMENTS

We are very thankful to the guide Lalico for field support in Maicá lake and to Francesca Nicole Angiolani-Larrea for providing photographs of the snake.

REFERENCES

  • 1
    Chippaux JP. Snakebite envenomation turns again into a neglected tropical disease! J Venom Anim Toxins. 2017;23:38.
  • 2
    Weinstein SA, Warrell DA, White J, Keyler DE. “Venomous” Bites from Non-Venomous Snakes: A Critical Analysis of Risk and Management of “Colubrid”. 1da ed. London: Elsevier; 2011. 336 p.
  • 3
    Prado-Franceschi J, Hyslop S. South American colubrid envenomations. Toxin Rev. 2002;21:117-58.
  • 4
    Ching A, Paes Leme AF, Zelanis A, Rocha MM, Furtado MdeF, Silva DA, et al. Venomics profling of Thamnodynastes strigatus unveils matrix metalloproteinases and other novel proteins recruited to the toxin arsenal of rear-fanged snakes. J Proteome Res. 2012;11(2):1152-62.
  • 5
    Weinstein SA, White J, Keyler DE, Warrell DA. Non-front-fanged colubroid snakes: a current evidence-based analysis of medical significance. Toxicon. 2013;69(2):103-13.
  • 6
    Diaz F, Navarrete LF, Pefaur J, Rodrigues-Acosta A. Envenomation by neotropical opistoglyphous colubrid Thamnodynastes cf. pallidus Linneé, 1758 (Serpentes: Colubridae) in Venezuela. Rev Inst Med Trop São Paulo. 2004;46(5):287-90.
  • 7
    Araújo PF, Silva WM, França RC, França FGR. A case of envenomation by neotropical Ophisthoglyphous snake Thamnodynastes pallidus (Linnaeus, 1958) (Colubridae: Dipsadinae: Tachymenini) in Brazil. Rev Inst Med Trop São Paulo . 2018;38:1-4.
  • 8
    Bailey JR, Thomas RA, Silva-Jr NJ. A revision of the South American snake genus Thamnodynastes Wagler, 1830 (Serpentes, Colubridae, Tachymenini). I. Two new species of Thamnodynastes from Central Brazil and adjacent areas, with a redefinition of and neotype designation for Thamnodynastes pallidus (Linnaeus, 1758). Phyllomedusa. 2005;4:83-101.
  • 9
    Fry BG, Winkel KD, Wickramaratna JC, Hodgson WC, Wüster W. Effectiveness of snake antivenom: species and regional variation and its clinical impact. Journal of Toxicology. Toxin Rev . 2003;22(1):23-34.
  • 10
    Bolon I, Durso AM, Botero Mesa S, Ray N, Alcoba G, Chappuis F, et al. Identifying the snake: First scoping review on practices of communities and healthcare providers confronted with snakebite across the world. PLoS ONE. 2020;15(3): e0229989.
  • 11
    Feitosa ES, Sampario V, Sachett J, Castro DB, Noronha MDN, Lozano JLL, et al. Snakebites as a largely neglected problem in the Brazilian Amazon: highlights of the epidemiological trends in the State of Amazonas. Rev Soc Bras Med Trop. 2015;48(Supl. 1):34-41.
  • 12
    Cupo P. Bites and stings from venomous animals: a neglected Brazilian tropical disease. Rev Soc Bras Med Trop . 2015;48(6):639-41.
  • Financial Support: This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Fiance Code 001, for PHSG (master’s degree scholarship), and RF (PNPD postdoc fellowship). LBVN received a scholarship from Fundação Amazônia de Amparo e Estudos e Pesquisas (FAPESPA).

Publication Dates

  • Publication in this collection
    13 Nov 2020
  • Date of issue
    2021

History

  • Received
    29 Apr 2020
  • Accepted
    29 May 2020
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