Bungarus multicinctus multicinctus Snakebite in Taiwan

Yan-Chiao Mao Division of Clinical Toxicology, Department of Emergency Medicine, Taichung Veterans General Hospital, Taichung, Taiwan.
Institute of Environmental and Occupational Health Sciences, School of Medicine, National Yang-Ming University, Taipei, Taiwan.
Division of Clinical Toxicology and Occupational Medicine, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan.
School of Medicine, National Defense Medical Center, Taipei, Taiwan.

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Po-Yu Liu Division of Infection, Department of Medicine, Taichung Veterans General Hospital, Taichung, Taiwan.

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Liao-Chun Chiang National Tsing Hua University, College of Life Sciences, Hsinchu, Taiwan.
National Health Research Institutes, National Institute of Infectious Diseases and Vaccinology, Miaoli, Taiwan.

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Shu-Chen Liao Institute of Environmental and Occupational Health Sciences, School of Medicine, National Yang-Ming University, Taipei, Taiwan.
Department of Emergency Medicine, Chang Guang Memorial Hospital, Taipei, Taiwan.

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Hung-Yuan Su Department of Emergency Medicine, E-Da Hospital, I-Shou University, Kaohsiung, Taiwan.

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Szu-Yin Hsieh Division of Clinical Toxicology, Department of Emergency Medicine, Taichung Veterans General Hospital, Taichung, Taiwan.

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Chen-Chang Yang Institute of Environmental and Occupational Health Sciences, School of Medicine, National Yang-Ming University, Taipei, Taiwan.
Division of Clinical Toxicology and Occupational Medicine, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan.

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Although specific antivenom is available in Taiwan, respiratory failure and general pain frequently accompany Bungarus multicinctus envenomation and there have been few reports on the management of B. multicinctus envenomation. We retrospectively analyzed 44 cases of B. multicinctus bite admitted to Taichung Veterans General Hospital (VGH) or to Taipei VGH. Demographic data, treatment, and outcome of patients with and without respiratory failure were compared. In this study, 20.5% patients had bites without noticeable signs or symptoms of significant envenoming, 27.3% developed respiratory failure, and 27.3% experienced general pain. Bivalent specific antivenom for B. multicinctus and N. atra was administered in all envenomed cases. Respiratory failure occurred 1.5–6.5 hours post-bite and general pain occurred 1–12 hours post-bite. Specific antivenom for B. multicinctus and N. atra at the recommended dose (i.e., 2–4 vials) might not effectively prevent respiratory failure and pain. Respiratory failure, general pain, and autonomic effects after B. multicinctus bite were probably caused, at least partly, by β-bungarotoxin. Although general weakness, ptosis, dysarthria, and dilated pupils were significantly associated with respiratory failure, their predictive value could not be accurately determined in such a retrospective study. Due to the rapid onset of respiratory failure, every suspected envenomed case thus should be closely monitored in the first few hours. We recommend the initial administration of four vials of antivenom in all envenomation cases, and a subsequent four vials be considered if the patient's condition is deteriorating. Prospective evaluation of the antivenom dosing regimen is urgently needed to improve B. multicinctus envenomation treatment.

Author Notes

* Address correspondence to Chen-Chang Yang, Division of Clinical Toxicology and Occupational Medicine, Department of Medicine, Taipei Veterans General Hospital, 201 Sec. 2, Shipai Road, Taipei 112, Taiwan. E-mail: ccyang@vghtpe.gov.tw

Authors' addresses: Yan-Chiao Mao, Division of Clinical Toxicology, Department of Emergency Medicine, Taichung Veterans General Hospital, Taichung, Taiwan, Institute of Environmental and Occupational Health Sciences, School of Medicine, National Yang-Ming University, Taipei, Taiwan, Division of Clinical Toxicology and Occupational Medicine, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan, and School of Medicine, National Defense Medical Center, Taipei, Taiwan, E-mail: doc1385e@gmail.com. Po-Yu Liu, Division of Infection, Department of Medicine, Taichung Veterans General Hospital, Taichung, Taiwan, E-mail: idfellow@gmail.com. Liao-Chun Chiang, National Tsing Hua University, College of Life Sciences, Hsinchu, Taiwan, and National Health Research Institutes, National Institute of Infectious Diseases and Vaccinology, Miaoli, Taiwan, E-mail: axe956956@gmail.com. Shu-Chen Liao, Institute of Environmental and Occupational Health Sciences, School of Medicine, National Yang-Ming University, Taipei, Taiwan, and Department of Emergency Medicine, Chang Guang Memorial Hospital, Taipei, Taiwan, E-mail: ermdsusan@yahoo.com.tw. Hung-Yuan Su, Department of Emergency Medicine, E-Da Hospital, I-Shou University, Kaohsiung, Taiwan, E-mail: hys927@hotmail.com. Szu-Yin Hsieh, Division of Clinical Toxicology, Department of Emergency Medicine, Taichung Veterans General Hospital, Taichung, Taiwan, E-mail: momohsieh@vghtc.gov.tw. Chen-Chang Yang, Institute of Environmental and Occupational Health Sciences, School of Medicine, National Yang-Ming University, Taipei, Taiwan, and Division of Clinical Toxicology and Occupational Medicine, Department of Medicine, Taipei Veterans General Hospital, Taipei, Taiwan, E-mail: ccyang@vghtpe.gov.tw.

  • 1.

    Mao YC, Hung DZ, 2015. Epidemiology of snake envenomation in Taiwan. Clinical Toxinology in Asia Pacific and Africa. Singapore: Springer, 322.

  • 2.

    Mao YC, Hung DZ, 2015. Management of snake envenomation in Taiwan. Clinical Toxinology in Asia Pacific and Africa. Singapore: Springer, 2352.

  • 3.

    Uetz P, Freed P, Hošek J, (eds), 2016. The Reptile Database. Available at: http://www.reptile-database.org. Accessed February 1, 2017.

  • 4.

    Pe T, Myint T, Htut A, Htut T, Myint AA, Aung NN, 1997. Envenoming by Chinese krait (Bungarus multicinctus) and banded krait (B. fasciatus) in Myanmar. Trans R Soc Trop Med Hyg 91: 686688.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Sawai Y, Kawamura Y, Toriba M, Kobayashi T, Wang NP, Li CB, Li ZY, Li HP, Tang SX, 1992. An epidemiological study on the snakebites in Guangxi Zhuang autonomous region, China in 1990. The Snake 24: 115.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Kuo TP, Wu CS, 1972. Clinico-pathological studies on snakebites in Taiwan. J Formos Med Assoc 71: 447466.

  • 7.

    Hung HT, Hojer J, Du NT, 2009. Clinical features of 60 consecutive ICU-treated patients envenomed by Bungarus multicinctus. Southeast Asian J Trop Med Public Health 40: 518524.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Hung DZ, Wu TC, Deng JF, 1997. The painful experience of inappropriate therapy of snake bites: a report of two cases. Zhonghua Yi Xue Za Zhi (Taipei) 60: 326330.

  • 9.

    Silva A, Maduwage K, Sedgwick M, Pilapitiya S, Weerawansa P, Dahanayaka NJ, Buckley NA, Johnston C, Siribaddana S, Isbister GK, 2016. Neuromuscular effects of common krait (Bungarus caeruleus) envenoming in Sri Lanka. PLoS Negl Trop Dis 10: e0004368.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Hung DZ, Wu ML, Deng JF, Lin-Shiau SY, 2002. Russell's viper snakebite in Taiwan: differences from other Asian countries. Toxicon 40: 12911298.

  • 11.

    Myint L, Warrell DA, Phillips RE, Tin Nu S, Tun P, Maung Maung L, 1985. Bites by Russell's viper (Vipera russelli siamensis) in Burma: haemostatic, vascular, and renal disturbances and response to treatment. Lancet 2: 12591264.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Wang W, Chen QF, Yin RX, Zhu JJ, Li QB, Chang HH, Wu YB, Michelson E, 2014. Clinical features and treatment experience: a review of 292 Chinese cobra snakebites. Environ Toxicol Pharmacol 37: 648655.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Mao YC, Liu PY, Hung DZ, Lai WC, Huang ST, Hung YM, Yang CC, 2016. Bacteriology of Naja atra snakebite wound and its implications for antibiotic therapy. Am J Trop Med Hyg 94: 11291135.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Whitaker R, Whitaker S, 2012. Venom, antivenom production and the medically important snakes of India. Curr Sci 103: 635643.

  • 15.

    Nelson L, Shawn L, 2012. Case studies in toxicology: descending paralysis ascending the path to diagnosis. Emergency Medicine-Chatham 44: 4.

  • 16.

    Sobel J, 2005. Botulism. Clin Infect Dis 41: 11671173.

  • 17.

    Nirthanan S, Gwee MC, 2004. Three-finger alpha-neurotoxins and the nicotinic acetylcholine receptor, forty years on. J Pharmacol Sci 94: 117.

  • 18.

    Rowan EG, 2001. What does β-bungarotoxin do at the neuromuscular junction. Toxicon 39: 107118.

  • 19.

    Chiappinelli VA, 1983. Kappa-bungarotoxin: a probe for the neuronal nicotinic receptor in the avian ciliary ganglion. Brain Res 277: 922.

  • 20.

    Chang LS, Chung C, Wu BN, Yang CC, 2002. Characterization and gene organization of Taiwan banded krait (Bungarus multicinctus) gamma-bungarotoxin. J Protein Chem 21: 223229.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Chiappinelli V, 1991. κ-Neurotoxins and α-neurotoxins: effects on neuronal nicotinic acetylcholine receptors. Snake toxins. New York, NY: Pergamon Press, 223258.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Chang CC, Lee CY, 1963. Isolation of neurotoxins from the venom of Bungarus multicinctus and their modes of neuromuscular blocking action. Arch Int Pharmacodyn Ther 144: 241257.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Kondo K, Toda H, Narita K, Lee CY, 1982. Amino acid sequences of three beta-bungarotoxins (beta 3-, beta 4-, and beta 5- bungarotoxins) from Bungarus multicinctus venom. Amino acid substitutions in the A chains. J Biochem 91: 15311548.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Aird SD, Womble GC, Yates JR 3rd, Griffin PR, 1999. Primary structure of gamma-bungarotoxin, a new postsynaptic neurotoxin from venom of Bungarus multicinctus. Toxicon 37: 609625.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Lee CY, Chang SL, Kau ST, Luh SH, 1972. Chromatographic separation of the venom of Bungarus multicinctus and characterization of its components. J Chromatogr A 72: 7182.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Prasarnpun S, Walsh J, Awad SS, Harris JB, 2005. Envenoming bites by kraits: the biological basis of treatment-resistant neuromuscular paralysis. Brain 128: 29872996.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Harris JB, Scott-Davey T, 2013. Secreted phospholipases A2 of snake venoms: effects on the peripheral neuromuscular system with comments on the role of phospholipases A2 in disorders of the CNS and their uses in industry. Toxins (Basel) 5: 25332571.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Lee CY, Tseng LF, 1966. Distribution of Bungarus multicinctus venom following envenomation. Toxicon 3: 281290.

  • 29.

    Gutierrez JM, Leon G, Lomonte B, 2003. Pharmacokinetic-pharmacodynamic relationships of immunoglobulin therapy for envenomation. Clin Pharmacokinet 42: 721741.

  • 30.

    Hung HT, Höjer J, Kiem TX, Du NT, 2010. A controlled clinical trial of a novel antivenom in patients envenomed by Bungarus multicinctus. J Med Toxicol 6: 393397.

  • 31.

    Chiappinelli VA, Wolf KM, 1989. Kappa-neurotoxins: heterodimer formation between different neuronal nicotinic receptor antagonists. Biochemistry 28: 85438547.

  • 32.

    Pillai LV, Ambike D, Husainy S, Khaire A, Captain A, Kuch U, 2012. Severe neurotoxic envenoming and cardiac complications after the bite of a ‘Sind Krait’ (Bungarus cf. sindanus) in Maharashtra, India. Trop Med Health 40: 103108.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Ariaratnam CA, Sheriff MH, Theakston RD, Warrell DA, 2008. Distinctive epidemiologic and clinical features of common krait (Bungarus caeruleus) bites in Sri Lanka. Am J Trop Med Hyg 79: 458462.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Kuch U, Sharma SK, Alirol E, Chappuis F, 2011. Fatal neurotoxic envenomation from the bite of a lesser black krait (Bungarus lividus) in Nepal. Southeast Asian J Trop Med Public Health 42: 960964.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Theakston RD, Phillips RE, Warrell DA, Galagedera Y, Abeysekera DT, Dissanayaka P, de Silva A, Aloysius DJ, 1990. Envenoming by the common krait (Bungarus caeruleus) and Sri Lankan cobra (Naja naja naja): efficacy and complications of therapy with Haffkine antivenom. Trans R Soc Trop Med Hyg 84: 301308.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Warrell DA, Looareesuwan S, White NJ, Theakston RD, Warrell MJ, Kosakarn W, Reid HA, 1983. Severe neurotoxic envenoming by the Malayan krait Bungarus candidus (Linnaeus): response to antivenom and anticholinesterase. Br Med J (Clin Res Ed) 286: 678680.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Faiz A, Ghose A, Ahsan F, Rahman R, Amin R, Hassan MU, Chowdhury AW, Kuch U, Rocha T, Harris JB, Theakston RD, Warrell DA, 2010. The greater black krait (Bungarus niger), a newly recognized cause of neuro-myotoxic snake bite envenoming in Bangladesh. Brain 133: 31813193.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Appiah-Ankam J, Hunter JM, 2004. Pharmacology of neuromuscular blocking drugs. Contin Educ Anaesth Crit Care Pain 4: 27.

  • 39.

    Nasseri K, Arvien S, 2016. Effects of low-dose ketamine on succinylcholine-induced postoperative myalgia in outpatient surgeries: a randomized, double-blind study. J Pain Res 9: 503508.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    White DC, 1962. Observations on the prevention of muscle pains after suxamethonium. Br J Anaesth 34: 332335.

  • 41.

    McLoughlin C, Elliott P, McCarthy G, Mirakhur R, 1992. Muscle pains and biochemical changes following suxamethonium administration after six pretreatment regimens. Anaesthesia 47: 202206.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Storella RJ, Schouchoff AL, Fujii M, Hill J, Fletcher JE, Jiang MS, Smith LA, 1992. Preliminary evidence for a postsynaptic action of beta-bungarotoxin in mammalian skeletal muscle. Toxicon 30: 349354.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Bawaskar HS, Bawaskar PH, Bawaskar PH, 2014. Premonitory signs and symptoms of envenoming by common krait (Bungarus caeruleus). Trop Doct 44: 8285.

  • 44.

    Laothong C, Sitprija V, 2001. Decreased parasympathetic activities in Malayan krait (Bungarus candidus) envenoming. Toxicon 39: 13531357.

  • 45.

    Muramatsu I, Fujiwara M, Miura A, Hayashi K, Lee C-Y, 1980. Beta-bungarotoxin and parasympathetic nerve blocking action. J Pharmacol Exp Ther 213: 156160.

  • 46.

    Chiappinelli VA, 1985. Actions of snake venom toxins on neuronal nicotinic receptors and other neuronal receptors. Pharmacol Ther 31: 132.

  • 47.

    Pinnock R, Lummis S, Chiappinelli V, Sattelle D, 1988. κ-bungarotoxin blocks an α-bungarotoxin-sensitive nicotinic receptor in the insect central nervous system. Brain Res 458: 4552.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Dando R, Roper SD, 2012. Acetylcholine is released from taste cells, enhancing taste signalling. J Physiol 590: 30093017.

  • 49.

    Hojer J, Tran Hung H, Warrell D, 2010. Life-threatening hyponatremia after krait bite envenoming: a new syndrome. Clin Toxicol (Phila) 48: 956957.

  • 50.

    Trinh KX, Khac QL, Trinh LX, Warrell DA, 2010. Hyponatraemia, rhabdomyolysis, alterations in blood pressure and persistent mydriasis in patients envenomed by Malayan kraits (Bungarus candidus) in southern Viet Nam. Toxicon 56: 10701075.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Simpson ID, Norris RL, 2007. Snake antivenom product guidelines in India: “The devil is in the details.” Wilderness Environ Med 18: 163168.

  • 52.

    World Health Organization Regional Office for South-East Asia, 2016. Guidelines for the Management of Snake-bites. New Delhi, India: World Health Organization Regional Office for South-East Asia.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    Otero R, Gutierrez JM, Rojas G, Nunez V, Diaz A, Miranda E, Uribe AF, Silva JF, Ospina JG, Medina Y, Toro MF, Garcia ME, Leon G, Garcia M, Lizano S, De La Torre J, Marquez J, Mena Y, Gonzalez N, Arenas LC, Puzon A, Blanco N, Sierra A, Espinal ME, Lozano R, 1999. A randomized blinded clinical trial of two antivenoms, prepared by caprylic acid or ammonium sulphate fractionation of IgG, in Bothrops and Porthidium snake bites in Colombia: correlation between safety and biochemical characteristics of antivenoms. Toxicon 37: 895908.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 54.

    de Silva HA, Ryan NM, de Silva HJ, 2016. Adverse reactions to snake antivenom, and their prevention and treatment. Br J Clin Pharmacol 81: 446452.

  • 55.

    Chen YC, Chen MH, Wang LM, Wu JJ, Huang CI, Lee CH, Yen DH, Yang CC, 2007. Antivenom therapy for crotaline snakebites: has the poison control center provided effective guidelines? J Formos Med Assoc 106: 10571062.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56.

    Chen JC, Bullard MJ, Chiu TF, Ng CJ, Liaw SJ, 2000. Risk of immediate effects from F(ab)2 bivalent antivenin in Taiwan. Wilderness Environ Med 11: 163167.

  • 57.

    Lin CC, Chaou CH, Tseng CY, 2015. An investigation of snakebite antivenom usage in Taiwan. J Formos Med Assoc 115: 672677.

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