Profile
International Journal of Clinical Research & Trials Volume 4 (2019), Article ID 4:IJCRT-133, 07 pages
https://doi.org/10.15344/2456-8007/2019/133
Scoping Study
Cerebrovascular Accident and Snake Envenomation: A Scoping Study

Mohammed Al-Sadawi1, Maliheh Mohamadpour1, Angelina Zhyvotovska1, Tahir Ahmed1,2, Joshua Schechter2, Yasmin Soliman1 and Samy I. McFarlane1,*

1Division of Cardiovascular Disease, Department of Internal Medicine, State University of New York, Downstate Medical Center, Brooklyn, NY 11203, USA
2Department of Emergency Medicine State University of New York, Downstate Medical Center, Brooklyn, New York, USA
Prof. Samy I. McFarlane, Divisions of Cardiovascular Disease,and Endocrinology, Department of Internal Medicine, State University of New York, Downstate Medical Center, Brooklyn, New York,11203, USA, Tel: 718- 270-6707, Fax: 718-270-4488; E-mail: smcfarlane@downstate.edu
22 December 2018; 09 April 2019; 11 April 2019
Al-Sadawi M, Mohamadpour M, Zhyvotovska A, Ahmed T, Schechter J, et al. (2019) Cerebrovascular Accident and Snake Envenomation: A Scoping Study. Int J Clin Res Trials 4: 133. doi: https://doi.org/10.15344/2456-8007/2019/133

Abstract

Background: Snake envenomation is associated with serious complications including infections, bleeding and, in rare occasions, thrombosis. Previous work by our group examined the association of snakebite and acute myocardial infarction. In this systematic review we aim to assess the clinical characteristics and outcomes of acute cerebrovascular accidents that are reported to be extremely rare complications of snake envenomation.
Methods: We performed a literature search for reports on stroke associated with snake envenomation between Jan 1995 to Oct 2018, and summarized their characteristics.
Results: Eighty-three published cases were reviewed. 66.3% of the cases were younger than 50 years of age. The mean time for the onset of the symptoms is 23.8±10.9 hours after exposure. 77.1% of the cases found to have ischemic stroke, 20.5% with intra-cranial hemorrhage and both infarction and hemorrhage in 2.4%. Mortality was reported in 16.9% with mean time between onset of the symptoms and death is 4.2 days.
Conclusion: Stroke secondary to snake envenomation is a rare but serious complication. Once stroke is suspected, initiating appropriate management is crucial in reducing morbidity and mortality associated with this potentially fatal complication of snake envenomation.


1. Introduction

Snake bite is one of the causes of stroke that has been reported less frequently. According to WHO, annual rate of snake bites have been estimated 5.4 million worldwide. Proximately 81000-138000 deaths have been reported annually. Most common affected population is among young adults and children in Africa, Asia and Latin America [1]. According to Center of Disease Control (CDC), annual rate of snake bite in the United States is 7,000-8,000 with about 5 deaths. The most common species in the United States reported by Central of Disease Control (CDC) includes rattlesnakes, copperheads, cottonmouths/water moccasins, and coral snakes [2]. In a Sri Lanka case series, the incidence of post-bite ischemic stroke was reported 9 in 500 bites [3].

Different Snake venoms contain different types of enzymes such as phospholipase A2, acetylcholinesterase, hyaluronidase, and metalloproteinases; such enzymes that have either direct neurotoxic or procoagulant or anticoagulation effects [4]. Therefore, These enzymes predisposing for causing either cerebral infarction due to cerebral hypoperfusion (watershed infarct), thrombotic occlusion of large vessels, vasculitis, consumption coagulopathy, or cardiogenic brain embolism; or hemorrhagic stroke [5,6].

Depending on the enzyme content in the venom, the procoagulation versus anticoagulation activities can be prominent. For Instance, viper and colubrid venoms contain metalloproteinases, serine proteases, and C-type lentins with either agonist or antagonist platelet aggregation activity while the venom of elapids contains phospholipase A2 and three-finger proteins, which acts as an neurotoxins in neuromuscular junction [7].

There are few case series reporting snakebite related strokes with detailed information regarding the type of the venom and the type of stroke. Previous work by our group examined the association of snakebite and acute myocardial infarction [8]. In this study, we reviewed different case reports and series of snake envenomation associated with stroke and the outcome.

2. Methods

On October 2018, a systematic search was conducted using PubMed and Google Scholar to review case reports about stroke caused by snake envenomation from January 1995 to October 2018. Studies that listed the keywords “snake, envenomation, stroke, cerebrovascular accidents” were used to identify case reports of stroke associated with snake envenomation. The reference list of each report was checked for additional cases. Data reviewed included demographic data, cardiovascular risk factors, snake species, computed tomography of the head, magnetic resonance of the head, time of presentation, complications, management, and outcome.

3. Results

83 cases were identified (Table 1) [9-79]. The patients were in the age group of 5 to 80 years and the mean age was 40 ± 17.5 years, median age was 40 years and 66.3% of the cases were younger than 50 years of age. 68.7% of the cases were reported for males and 31.3% for females. Diabetes Mellites and hypertension were reported only in 2 cases (2.4%). Snake Species are represented in (Figure 1); however, about 30% of the cases did not mention snake species. 30% of the cases reported with Daboia, Russell's viper, species. 83.1% of the cases were bitten in their legs and 16.9% were bitten in hands. All the cases were managed by anti-snake venom, in 27.7% of the cases the symptoms started after receiving anti-snake venom. 19.3% of the cases also treated with antiplatelet and 3.6% were treated with craniotomy. The mean time for the onset of the symptoms is 23.8±10.9 hours after exposure. 77.1% of the cases found to have ischemic stroke, 20.5% with intra-cranial hemorrhage and both infarction and stroke in 2.4%.

table 1
Table 1: Cases reported with snake envenomation associated with stroke [9-78].
figure 1
Figure 1: Frequency of Stroke envenomation by species. Note: 30% of the cases had no information regarding snake species.

Complications were reported in many cases: Altered mental status necessities intubation in 36.1% of the cases, acute kidney injury was reported in 12.2%, pulmonary edema in 3.6%, myocarditis in 1.2% and endocarditis in 1.2%. The outcome of the cases showed full recovery in 26.5% with mean time needed for recovery 88.9 days. Mortality was reported in 16.9% mainly due to complication of stroke with mean time between onset of the symptoms and death is 4.2 days.

4. Discussion

Venomous snakes can cause stroke due to either their neurotoxic or hemotoxic enzymes [4]. However, type of stroke either hemorrhagic or ischemic depends on the venom enzyme-make up in each different snake species.

Ischemic strokes were 77.1% of the cases while ICH were 20.5%. As reported, the most common species were Russell's vipers with higher incidence of ischemic stroke than intracranial hemorrhage (ICH). Whereas, reportedly Bothrops species were the second most common venoms to be reported with significantly more propensity towards ICH than ischemic stroke [3]. Most of the cases exposed to snake bites are young males <50 years old. Mortality rate was higher among Russell's vipers; however, Russell's vipers were the most commonly reported bite. There was single report of bite by Horned viper and Pseudonaja textilis with ICH; Cerastes and Deinagkistrodon envenomation were associated with large infarcts [29,74,32,66].

The venom of Bothrops species contains metalloproteinases, type of hemotoxin that can cause hemolysis, thrombocytopenia, disseminated intravascular coagulation [76,77]. Among Borthrops, ICH was frequently reported in jararacussu, atrox, marajoensis species and infarcts was reported for lanceolatu species. Most of the patient who had bites were young and no comorbidity or risk factor for either hemorrhagic or ischemic stroke except 2% who had history of diabetesmellitus or hypertension.

Mortality was more common among those who either arrived in coma or required intubation due to AMS during the course of hospitalization. Death happened within the first 4.2 days after the exposure. Risk of mortality was amplified by ICH, bilateral extensive cerebral, cerebellar infarction, mass effect, or post circulation occlusion.

However, all the cases received anti-venom once they sought medical care after exposure; while mean time for the onset of symptoms was 23.8 h after envenomation. In 27.7% of the cases symptoms started even after receiving antivenom which indicates the potency of the venom in causing stroke and the importance of early administration of anti-venom serum with consideration of other adjutant therapies. There are some animal studies indicating the critical and time sensitive usage of metalloproteinase inhibitors and antivenom would be the best approach to reduce hemorrhagic stroke after Bothrops species envenoming [78]. Studies have shown that single individual fractions of different venoms have failed to be lethal to mice in some studies even after 48 h, whereas a corresponding concentration of whole crude venom have been sufficiently lethal within 10 min. Synergistic action of venom component is important for designing more effective antivenoms [79]. In figure 2, we summarized the postulated mechanisms for cerebrovascular accidents following a snake envenomation.

figure 2
Figure 2: Postulated mechanisms for cerebrovascular accidents following a snake bite.

Limited access to antivenom and also lack of awareness for seeking medical management shortly after snakebite to reduce the chance of cerebrovascular events and the other complications mainly in developing countries is an alarming medical emergency to be addressed. Therefore, WHO considered snake envenomation as category A neglected tropical diseases to maximize the efforts facing its complication [80].

5. Conclusion

Stroke is a rare but rather serious complication of snake envenomation that is associated with high mortality rate. Further research is needed to elucidate the mechanisms of stroke in the context of snakebites thus paving the way for the development of specific therapeutic interventions. However, early administration of anti-venom serum with consideration of other adjutant therapies is crucial in snakebites in order to reduce the associated complications including strokes.

Competing Interests

The authors declare that they have no competing interests.

Acknowledgments

This work is supported, in part, by the efforts of Dr. Moro O. Salifu M.D., M.P.H., M.B.A., M.A.C.P., Professor and Chairman of Medicine through NIH Grant number S21MD012474.


References

  1. World Health Organization (2018) Facts sheets: WHO Snakebite envenoming [View]
  2. Center of Disease Control
  3. Thomas L, Tyburn B, Ketterlé J, Biao T, Mehdaoui H, et al. (1998) Prognostic significance of clinical grading of patients envenomed by Bothrops lanceolatus in Martinique. Soc Trop Med Hyg 92: 542-545 [CrossRef] [Google Scholar] [PubMed]
  4. Warrell DA (1996) Animal toxins. In: Cook GC, ed. Manson’s tropical diseases. 20th ed. London: Saunders
  5. Del Brutto OH (2013) Neurological effects of venomous bites and stings: snakes, spiders, and scorpions. HandbClin Neurol 114: 349-368 [CrossRef] [Google Scholar] [PubMed]
  6. Panicker JN, Madhusudanan S (2000) Cerebral infarction in a young male following viper envenomation. J Assoc Physicians India 48: 744-745 [Google Scholar] [PubMed]
  7. Del Brutto OH, Del Brutto VJ (2012) Neurological complications of venomous snake bites: a review. Acta Neurol Scand 125: 363-372 [CrossRef] [Google Scholar] [PubMed]
  8. Samy I McFarlane (2018) Myocardial Infarction after Snakebite Envenomation: A Scoping Study. SF J Cardiol 2:3 [Google Scholar] [PubMed]
  9. Sahoo AK, Sriramka B (2018) Acute Reversible Ischemic Stroke after Snake Bite. Indian J Crit Care Med 22: 611-612 [CrossRef] [Google Scholar] [PubMed]
  10. Sahoo LK, Mallick AK, Mohanty G, Swain KP, Biswal NR, et al. (2018) A Rare Case of Stroke Due to Multiple Ischemic Infarctions following Russell's Viper Envenomation. Med J DY Patil Vidyapeeth 11: 57-58 [Google Scholar]
  11. Kutiyal AS, Malik C, Hyanki G (2018) Locked-in syndrome post snake bite: a rare presentation. Trop Doct 48: 68-69 [CrossRef] [Google Scholar] [PubMed]
  12. Pothukuchi VK, Chepuri VR, Natta K, Madigani N, Kumar A, et al. (2017) A rare case report of Russell’s viper snakebite with ischemic stroke. Hong Kong Journal of Emergency Medicine 25: 95-97 [CrossRef] [Google Scholar]
  13. Bakare AK, Wahab K, Ilesanmi O, Sanya E (2018) Intraparenchymal Intracerebral Hemorrhage Complicating Venomous Snakebite in Nigeria: A Case Report. Neurology 90: 6.235 [Google Scholar]
  14. Pothukuchi VK, Kumar A, Teja C, Verma A (2017) Rare Case Series of Ischemic Stroke Following Russell’s Viper Snake Bite in India. Acta Med Indones 49: 343-346 [Google Scholar] [PubMed]
  15. Namal Rathnayaka RM, Kularatne SA, Kumarasinghe KD, Ranaweera J, Nishanthi Ranathunga PE, et al. (2017) Ischemic brain infarcts and intracranial haemorrhages following Russell’s viper (Daboiarusselii) bite in Sri Lanka. Toxicon 125: 70-73 [CrossRef] [Google Scholar] [PubMed]
  16. Delgado ABT, Gondim CCVL, Reichert LP, da Silva PHV, Souza RMDCE, et al. (2017) Hemorrhagic stroke secondary to Bothrops spp. venom: A case report. Toxicon 132: 6-8 [CrossRef] [Google Scholar] [PubMed]
  17. Silva de Oliveira S, Freitas-de-Sousa LA, Alves EC, de Lima Ferreira LC, da Silva IM, et al. (2017) Fatal stroke after Bothrops snakebite in the Amazonas state, Brazil: A case report. Toxicon 138: 102-106 [CrossRef] [Google Scholar] [PubMed]
  18. Janardanaaithala (2017) Thrombotic stroke following viper bite. University Journal of Medicine and Medical Sciences
  19. Swati AC, Arjun MD, Piyush AR (2017) Rare Snake Bite Sequelae: Intracerebral Haemorrhage with Cerebellar Infarction. International Journal of Contemporary Medical Researc
  20. Paul R, Sasane S (2017) Rare Ischemic Stroke Presentation after Viper Bite-A Case Report. Int.J Neurology Res [Google Scholar]
  21. Krishna PV, Ahmed S, Reddy KVN (2017) Ischemic stroke consequent to snake bite. J NTR Univ Health Sci 6: 192-193 [Google Scholar]
  22. Pal J, Mondal S, Sinha D, Ete T, Chakraborty A, et al. (2014) Cerebral infarction: an unusual manifestation of viper snake bite. IJRMS 2: 3 [Google Scholar]
  23. Thomas A, Varghese P, Jalal MJA (2017) Intracerebral Hemorrhage: A Rare Snake Bite Sequelae. Indian Journal of Neurosurgery 6: 27-30 [Google Scholar]
  24. Cañas CA (2016) Brainstem ischemic stroke after to Bothropsatrox snakebite, Toxicon 120: 124-127 [CrossRef] [Google Scholar] [PubMed]
  25. Silveira GG, Machado CR, Tuyama M, Lima MA (2016) Intracranial Bleeding Following Bothrops sp. Snakebite. Neurologist 21: 11-12 [CrossRef] [Google Scholar] [PubMed]
  26. Ajit D, Kumar SG (2016) Acute Cerebral Infarct on Evolution in Middle Cerebral Artery Following Viper Snake Bite. IJSR [CrossRef] [Google Scholar]
  27. Bhojaraja M, Prabhu MM, Stanley W, Sanket S, Marimuthu VKN, et al. (2016) Snake bite: An unusual cause of ischaemic stroke. AMJ 9: 138-141 [CrossRef] [Google Scholar]
  28. Jeyaraj M (2016) An interesting case of Ischemic stroke following snake bite. University Journal of Medicine and Medical Sciences 2: 1 [Google Scholar]
  29. Ghezala HB, Snouda S (2015) Accident vasculaire cerebral hémorragique mortel suite à une envenimation par une vipère à corne en Tunisie. Hemorrhagic stroke following a fatal envenomation by a horned viper in Tunisia. Pan Afr Med J 21: 156 [CrossRef] [Google Scholar] [PubMed]
  30. Pardal, Pinheiro, Silva, Santos, Gadelha. Hemorrhagic stroke in children caused by Bothropsmarajoensis envenoming: a case report. Journal of Venomous Animals and Toxins Including Tropical Diseases [Google Scholar]
  31. Paul G, Paul B, Puri S (2014) Snake bite and stroke: Our experience of two cases. Indian J Crit Care Med 18: 257-258 [CrossRef] [Google Scholar] [PubMed]
  32. Rebahi H, Nejmi H, Abouelhassan T, Hasni K, Samkaoui MA, et al. (2014) Severe Envenomation by Cerastescerastes Viper: An Unusual Mechanism of Acute Ischemic Stroke. J Stroke Cerebrovasc Dis 23: 169-172 [CrossRef] [Google Scholar] [PubMed]
  33. Bush SP, Mooy GG, Phan TH (2014) Catastrophic Acute Ischemic Stroke After Crotalidae Polyvalent Immune Fab (Ovine)-Treated Rattlesnake Envenomation. Wilderness Environ Med 25: 198-203 [CrossRef] [Google Scholar] [PubMed]
  34. Mahale R, Mehta A, Javali M, Srinivasa R (2014) A case of bilateral occipital lobe infarcts following Indian tree viper bite. J Stroke 16: 205-207 [CrossRef] [Google Scholar] [PubMed]
  35. Gopalan S, Ramadurai S, Bharathi L, Arthur P (2014) Ischaemic stroke with internal carotid artery occlusion following viper bite: A case report. Neurology Asia 19: 191-193 [Google Scholar]
  36. Chandrashekar, Anikethana GV, Kalinga BE (2012) Viper Bite Presenting as Acute Ischemic Stroke. IJSR [Google Scholar]
  37. Kumar N, Mukherjee S, Patel MP, Shah KB, Kumar S, et al. (2014) A case of saw scale viper snake bite presenting as intraparenchymal haemorrhage: case report. Int J Health Sci Res 4: 333-337 [Google Scholar]
  38. Vale TC, Leite AF, Hora PR, Coury MI, Silva RC, et al. (2013) Bilateral posterior circulation stroke secondary to a crotalid envenomation: case report. Rev Soc Bras Med Trop 46: 255-256 [CrossRef] [Google Scholar] [PubMed]
  39. Bhatt A, Menon AA, Bhat R, Ramamoorthi K (2013) Myocarditis along with acute ischaemic cerebellar, pontine and lacunar infarction following viper bite. BMJ Case Rep [CrossRef] [Google Scholar] [PubMed]
  40. Das SK, Khaskil S, Mukhopadhyay S, Chakrabarti S (2013) A patient of Russell's viper envenomation presenting with cortical venous thrombosis: An extremely uncommon presentation. J Postgrad Med 59: 235-236 [CrossRef] [Google Scholar] [PubMed]
  41. Aissaoui, Hammi, Chkoura (2013) Bull. Soc Pathol Exot 106: 163
  42. Saha K, Saha D, Mondal RRS, Ranjit P Sarkar S, et al. (2013) Cerebral Infarct with Septicemia: An unusual presentation of Snake Bite. IJRRMS [Google Scholar]
  43. Ittyachen AM, Jose MB (2012) Thalamic infarction following a Russell's viper bite. Southeast Asian J Trop Med Public Health 43: 1201-1204 [Google Scholar] [PubMed]
  44. Chani, Abouzahir, Haimeur, DrissiKamili, Mion, et al. Accident vasculairecérébralischémique à la suite d’uneenvenimationvipérine grave au Maroc, traitée par un antivenin inadapté. AnnalesFrançaisesd’Anesthésieet de Réanimation, 31: 82-85 [Google Scholar]
  45. Jeevagan V, Chang T, Gnanathasan CA (2012) Acute ischemic stroke following Hump-nosed viper envenoming; first authenticated case. Thromb 10: 21 [CrossRef] [Google Scholar] [PubMed]
  46. Gupta S, Tewari A, Nair V (2012) Cerebellar infarct with neurogenic pulmonary edema following viper bite. J Neurosci Rural Pract 3: 74-76 [CrossRef] [Google Scholar] [PubMed]
  47. Gouda S, Pandit V, Seshadri S, Valsalan R, Vikas M, et al. (2011) Posterior circulation ischemic stroke following Russell's viper envenomation. Ann Indian Acad Neurol 14: 301-303 [CrossRef] [Google Scholar] [PubMed]
  48. Deepu D, Hrishikesh S, Suma MT, Zoya V (2011) Posterior fossa infarct following Viper bite: a paradox. J Venom Anim Toxins incl Trop Dis 17: 358- 360 [CrossRef] [Google Scholar]
  49. Sathishkumar (2017). JMSCR
  50. Hsaini Y, Satte A, Balkhi H, Karouache A, Bourezza A, et al. (2010) Infarctus cerebral secondaire à une morsure de vipère. Annales Françaisesd’ Anesthésieet de Réanimation 29: 315-316 [View]
  51. Machado AS, Barbosa FB, Mello GS, Pardal PPO (2010) Hemorrhagic stroke related to snakebite by bothrops genus: a case report. Rev Soc Bras Med Trop 43: 602-604 [CrossRef] [Google Scholar] [PubMed]
  52. Tungpakorn N (2010) Unusual visual loss after snakebite. J Venom Anim Toxins incl Trop Dis 16: 519-523 [CrossRef] [Google Scholar]
  53. Narang SK, Paleti S, Azeez Asad MA, Samina T (2009) Acute ischemic infarct in the middle cerebral artery territory following a Russell's viper bite. Neurol India 57: 479-480 [CrossRef] [Google Scholar] [PubMed]
  54. Hoskote SS, Iyer VR, Kothari VM, Sanghvi DA (2009) Bilateral anterior cerebral artery infarction following viper bite. J Assoc Physicians India 57: 67-69 [Google Scholar] [PubMed]
  55. Gawarammana I, Mendis S, Jeganathan K (2009) Acute ischemic strokes due to bites by Daboiarusselii in Sri Lanka - First authenticated case series. Toxicon 54: 421-428 [CrossRef] [Google Scholar] [PubMed]
  56. Mugundhan K, Thruvarutchelvan K, Sivakumar S (2008) Posterior circulation stroke in a young male following snake bite. J Assoc Physicians India 56: 713-714 [Google Scholar] [PubMed]
  57. Prakash S, Mathew C, Bhagat S (2008) Locked-in Syndrome in Snakebite. J Assoc Physicians India 56: 121-122 [Google Scholar] [PubMed]
  58. Santos-Soares PC, Bacellar A, Povoas HP, Brito AF, Santana DL, et al. (2007) Stroke and snakebite: case report. Arq Neuropsiquiatr 65: 341-344 [CrossRef] [Google Scholar] [PubMed]
  59. Das (2007) Acute ischemic stroke in a Young Girl After Viper Bite. OPJ
  60. Thomas L, Chausson N, Uzan J, Kaidomar S, Vignes R, et al. (2006) Thrombotic stroke following snake bites by the “Fer-de-Lance” Bothropslanceolatus in Martinique despite antivenom treatment: A report of three recent cases. Toxicon 48: 23-28 [CrossRef] [Google Scholar] [PubMed]
  61. Merle H, Donnio A, Ayeboua L, Plumelle Y, Smadja D, et al. (2005) Occipital Infarction Releaved by Quadrantanopsia Following Snakebite by BothropsLanceolatus. Am J Trop Med Hyg 73: 583-585 [Google Scholar] [PubMed]
  62. Bhalla A, Jain AP, Banait S, Jajoo UN, Kalantri SP, et al. (2004) Central retinal artery occlusion: an unusual complication of snakebite. J Venom Anim Toxins incl Trop Dis 10: 311-314 [Google Scholar]
  63. Lee, Hong, Kim, Kim, Ko (2004) Cerebral Infarction Following Snakebite. J Korean SocEmerg Med 15: 420-425
  64. Bartholdi D, Selic C, Meier J, Jung HH (2004) Viper snakebite causing symptomatic intracerebral haemorrhage. J Neurol 251: 889-891 [CrossRef] [Google Scholar] [PubMed]
  65. Boviatsis EJ, Kouyialis AT, Papatheodorou G, Gavra M, Korfias S, et al. (2003) Multiple Hemorrhagic Brain Infarcts After Viper envenomation. Am J Trop Med Hyg 68: 253-257 [Google Scholar] [PubMed]
  66. Zhang T, Wang Y, Ye P, Liu J, Cheng Y, et al. (2018) Three-dimensional computed tomography reconstructive diagnosis of snakebite-induced cerebral infarction. J Xray Sci Technol 26: 165-169 [CrossRef] [Google Scholar] [PubMed]
  67. Hung DZ, Wu ML, Deng JF, Yang DY, Lin-Shiau SY, et al. (2002) Multiple Thrombotic Occlusions of Vessels after Russell’s Viper Envenoming. Pharmacol Toxicol 91: 106-110 [CrossRef] [Google Scholar] [PubMed]
  68. Diaz (2003) Infarto cerebral y accidenteofídico. Acta Neurol Colomb 19: 75- 79 [View]
  69. Numeric P, Moravie V, Didier M, Chatot-Henry D, Cirille S et al. (2002) Multiple cerebral infarctions following a snakebite by Bothrops caribbaeus. Am J Trop Med Hyg 67: 287-288 [CrossRef] [Google Scholar] [PubMed]
  70. Pinho MAO, Burdmann EA (2001) Fatal Cerebral Hemorrhage and acute renal failure After Young Bothrops Jararcussus snake bite. Renal Failure 23: 269-277 [CrossRef] [Google Scholar]
  71. Lee BC, Hwang SH, Bae JC, Kwon SB, et al. (2001) Brainstem infarction following Korean viper bite. Neurology 56: 1244-1245 [CrossRef] [Google Scholar] [PubMed]
  72. Panicker JN, Madhusudanan S (2000) Cerebral infarction in a young male following viper envenomation. J Assoc Physicians India 48: 744-745 [Google Scholar] [PubMed]
  73. Singh S, Dass A, Jain S, Varma S, Bannerjee AK, et al. (1998) Fatal Non- Bacterial Thrombotic Endocarditis Following Viperine Bite. Intern Med 37: 342-344 [CrossRef] [Google Scholar] [PubMed]
  74. Midyett FA (1998) Neuroradiologic findings in brown snake envenomation: computed tomography demonstration. Australas Radiol 42: 248-249 [CrossRef] [Google Scholar] [PubMed]
  75. Cole M (1996) Cerebral Infarct After Rattlesnake Bite. Arch Neurol 53: 957- 958 [CrossRef] [Google Scholar] [PubMed]
  76. Rucavado A, Soto M, Kamiguti AS, Theakston RD, Fox JW, et al. Characterization of aspercetin, a platelet aggregating component from the venom of the snake Bothrops asper which induces thrombocytopenia and potentiates metalloproteinase-induced hemorrhage. Thromb Haemost 85: 710-715 [Google Scholar] [PubMed]
  77. Kamiguti AS, Cardoso JL (1989) Haemostatic changes caused by the venoms of South American snakes. Toxicon 27: 955-963 [CrossRef] [Google Scholar] [PubMed]
  78. Gutierrez JM, Leon G, Tojas G, Lomonte B, Rucavado A, et al. (1989) Neutralization of local tissue damage induced by Bothrops asper (terciopelo) snake venom. Toxicon 36: 1529-1538 [CrossRef] [Google Scholar] [PubMed]
  79. Xiong S, Huang C (2018) Synergistic strategies of predominant toxins in snake venoms. Toxicol Lett 287: 142-154 [CrossRef] [Google Scholar] [PubMed]
  80. The Lancet (2007) Snake-bite envenoming: a priority neglected tropical disease. Lancet 390: 2 [CrossRef] [Google Scholar] [PubMed]