Wilderness & Environmental Medicine
Volume 21, Issue 1 , Pages 35-45 , March 2010

Sensationalistic Journalism and Tales of Snakebite: Are Rattlesnakes Rapidly Evolving More Toxic Venom?

  • William K. Hayes, PhD

      Affiliations

    • Department of Earth and Biological Sciences, Loma Linda University, Loma Linda, CA
    • Corresponding Author InformationCorresponding author: William K. Hayes, PhD, Department of Earth and Biological Sciences, Loma Linda University, Loma Linda, CA 92350
  • ,
  • Stephen P. Mackessy, PhD

      Affiliations

    • School of Biological Sciences, University of Northern Colorado, Greeley, CO

References 

  1. Myers AL. Rattlesnake bite victims showing extreme symptoms. Associated Press. 2008;24 May
  2. Nolan K. Is rattlesnake's bite growing deadlier?. The Arizona Republic. 2008;14 June
  3. Edwards K. Snakes in San Diego: potent, powerful venom cause for concern. UC San Diego Medical Center News Release http://health.ucsd.edu/news/2008/6-9-Toxicologist-advice.htmAccessed November 11, 2009
  4. Warth G. Snakebites becoming more toxic. North County Times. 2008;9 June
  5. Grenard S. Is rattlesnake venom evolving?. Nat Hist (Am Mus Nat Hist.). 2000;109:44–46
  6. Anon. Expert: rattlesnake species more deadly. United Press International. 2009;20 April
  7. LaFee S. Rattler's reputation takes a toxic turn for the worse. San Diego Union-Tribune. 2009;20 April
  8. Tennesen M. Snakebit. Sci Am. 2009;300:27–30
  9. Hayes WK, Herbert SS, Rehling GC, Gennaro J. Factors that influence venom expenditure in viperids and other snake species during predatory and defensive contexts. In:  Schuett GW,  Höggren M,  Douglas ME,  Greene HW editor. Biology of the Vipers. Eagle Mountain, UT: Eagle Mountain Publishing; 2002;p. 207–233
  10. Hayes WK. The snake venom-metering controversy: levels of analysis, assumptions, and evidence. In:  Hayes WK,  Beaman KR,  Cardwell MD,  Bush SP editor. The Biology of Rattlesnakes. Loma Linda, CA: Loma Linda University Press; 2008;p. 191–220
  11. Klauber LM. Rattlesnakes: Their Habits, Life Histories and Influence on Mankind. 2 vols 2nd ed.. Berkeley, CA: University of California Press; 1972;
  12. Mackessy SP, Williams K, Ashton KG. Ontogenetic variation in venom composition and diet of Crotalus oreganus concolor: a case of venom paedomorphosis?. Copeia. 2003;2003:769–782
  13. Hayes WK. Ontogeny of striking, prey-handling and envenomation behavior of prairie rattlesnakes (Crotalus v. viridis). Toxicon. 1991;29:867–875
  14. Herbert SS. Factors influencing venom expenditure during defensive bites by cottonmouths (Agkistrodon piscivorus) and rattlesnakes (Crotalus viridis, Crotalus atrox). [Masters thesis] Loma Linda, CA: Loma Linda University; 1998;
  15. Herbert SS. Venom expenditure by viperid and elapid snakes: mechanisms, adaptation, and application. [PhD dissertation] Loma Linda, CA: Loma Linda University; 2007;
  16. Herbert SS, Hayes WK. Denim clothing reduces venom expenditure by rattlesnakes striking defensively at model human limbs. Ann Emerg Med. 2009;54:830–836
  17. Hayes WK. Venom metering by juvenile prairie rattlesnakes (Crotalus v. viridis): effects of prey size and experience. Anim Behav. 1995;50:33–40
  18. Wingert WA, Chan L. Rattlesnake bites in southern California and rationale for recommended treatment. West J Med. 1988;148:37–44
  19. Hayes WK, Bush SP, Herbert SS, Rehling GC, Cardwell MD, Dugan EA. Defensive bites by rattlesnakes (genus Crotalus): venom expenditure, envenomation severity, and the importance of snake size. In: Program and Abstracts of the Biology of the Rattlesnakes Symposium. Loma Linda, CA: Loma Linda University; 2005;p. 31
  20. MacDonald GM, Stahle DW, Diaz JV, et al. Climate warming and 21st-century drought in southwestern North America. Eos Trans AGU. 2008;89:82–85
  21. Bradley RD, Hanson JD, Amman BR, et al. Rapid recovery of rodent populations following severe drought. Southwest Nat. 2006;51:87–93
  22. Beaupre SJ. Annual variation in time-energy allocation by timber rattlesnakes (Crotalus horridus) in relation to food acquisition. In:  Hayes WK,  Beaman KR,  Cardwell MD,  Bush SP editor. The Biology of Rattlesnakes. Loma Linda, CA: Loma Linda University Press; 2008;p. 111–122
  23. Cardwell MD. The reproductive ecology of Mohave rattlesnakes. J Zool. 2008;274:65–76
  24. Taylor EN, DeNardo DF. Proximate determinants of sexual size dimorphism in the western diamond-backed rattlesnake. In:  Hayes WK,  Beaman KR,  Cardwell MD,  Bush SP editor. The Biology of Rattlesnakes. Loma Linda, CA: Loma Linda University Press; 2008;p. 91–100
  25. Rehling GC. Venom expenditure in multiple bites by rattlesnakes and cottonmouths. [Masters thesis] Loma Linda, CA: Loma Linda University; 2002;
  26. Sanz L, Gibbs HL, Mackessy SP, Calvete JJ. Venom proteomes of closely related Sistrurus rattlesnakes with divergent diets. J Proteome Res. 2006;5:2098–2112
  27. Pahari S, Mackessy SP, Kini RM. The venom gland transcriptome of the desert massasauga rattlesnake (Sistrurus catenatus edwardsii): towards an understanding of venom composition among advanced snakes (superfamily Colubroidea). BMC Molec Biol. 2007;8:115
  28. Mackessy SP. Venom composition in rattlesnakes: trends and biological significance. In:  Hayes WK,  Beaman KR,  Cardwell MD,  Bush SP editor. The Biology of Rattlesnakes. Loma Linda, CA: Loma Linda University Press; 2008;p. 495–510
  29. Mackessy SP. The field of reptile toxinology: snakes, lizards and their venoms. In:  Mackessy SP editors. Handbook of Venoms and Toxins of Reptiles. Boca Raton, FL: Taylor & Francis/CRC Press; 2009;p. 3–23
  30. Fox JW, Shannon JD, Stefansson B, et al. Role of discovery science in toxicology: examples in venom proteomics. In:  Ménez A editors. Perspectives in Molecular Toxinology. West Sussex, UK: Wiley; 2002;p. 97–108
  31. Fox JW, Serrano SM. Exploring snake venom proteomes: multifaceted analyses for complex toxin mixtures. Proteomics. 2008;8:909–920
  32. Doley R, Pahari S, Mackessy SP, Kini RM. Accelerated exchange of exon segments in viperid three-finger toxin genes (Sistrurus catenatus edwardsii; desert massasauga). BMC Evol Biol. 2008;8:196
  33. Gibbs HL, Rossiter W. Rapid evolution by positive selection and gene gain loss: PLA2 venom genes in closely related Sistrurus rattlesnakes with divergent diets. J Mol Evol. 2008;66:151–166
  34. Juárez P, Comas I, González-Candelas F, Calvete JJ. Evolution of snake venom disintegrins by positive Darwinian selection. Mol Biol Evol. 2008;25:2391–2407
  35. Gibbs HL, Prior KA, Weatherhead PJ, Johnson G. Genetic structure of populations of the threatened eastern massasauga rattlesnake, Sistrurus c. catenatus: evidence from microsatellite DNA markers. Mol Ecol. 1997;6:1123–1132
  36. Holycross AT, Douglas ME. Geographic isolation, genetic divergence, and ecological non-exchangeability define ESUs in a threatened sky-island rattlesnake. Biol Cons. 2007;134:142–154
  37. Daltry JC, Wüster W, Thorpe RS. Diet and snake venom evolution. Nature. 1996;379:537–540
  38. Heatwole H, Poran N, King P. Ontogenetic changes in the resistance of bullfrogs (Rana catesbeiana) to the venom of copperheads (Agkistrodon contortrix contortrix) and cottonmouths (Agkistrodon piscivorus piscivorus). Copeia. 2000;2000:808–814
  39. Biardi JE. The ecological and evolutionary context of mammalian resistance to rattlesnake venoms. In:  Hayes WK,  Beaman KR,  Cardwell MD,  Bush SP editor. The Biology of Rattlesnakes. Loma Linda, CA: Loma Linda University Press; 2008;p. 557–568
  40. Gibbs HL, Mackessy SP. Functional basis of a molecular adaptation: prey-specific toxic effects of venom from Sistrurus rattlesnakes. Toxicon. 2009;53:672–679
  41. Mackessy SP. Venom ontogeny in the Pacific rattlesnakes Crotalus viridis helleri and Crotalus viridis oreganus. Copeia. 1988;1988:92–101
  42. Campbell JA, Lamar WW. The Venomous Reptiles of the Western Hemisphere. Ithaca, NY: Cornell University Press; 2004;
  43. Meik JM, Fontenot BE, Franklin CJ, King C. Apparent natural hybridization between the rattlesnakes Crotalus atrox and C. horridus. Southwest Nat. 2008;53:196–200
  44. Werman SD. Phylogeny and the evolution of β-neurotoxic phospholipases A2 (PLA2) in the venoms of rattlesnakes, Crotalus and Sistrurus (Serpentes: Viperidae). In:  Hayes WK,  Beaman KR,  Cardwell MD,  Bush SP editor. The Biology of Rattlesnakes. Loma Linda, CA: Loma Linda University Press; 2008;p. 511–536
  45. French WJ, Hayes WK, Bush SP, Cardwell MD, Bader JO, Rael E. Mojave toxin in venom of Crotalus helleri (southern Pacific rattlesnake): molecular and geographic characterization. Toxicon. 2004;44:781–791
  46. Bush SP, Siedenburg E. Neurotoxicity associated with suspected southern Pacific rattlesnake (Crotalus viridis helleri) envenomation. Wilderness Environ Med. 1999;10:247–249
  47. Richardson WH, Goto CS, Gutglass DJ, Williams SR, Clark RF. Rattlesnake envenomation with neurotoxicity refractory to treatment with crotaline Fab antivenom. Clin Toxicol. 2007;45:472–475
  48. Ferquel E, de Haro L, Jan V, et al. Reappraisal of Vipera aspis venom neurotoxicity. PLoS One. 2007;2:e1194
  49. Bush SP, Green SM, Moynihan JA, Hayes WK, Cardwell MD. Crotalidae polyvalent immune Fab (ovine) antivenom is efficacious for envenomations by Southern Pacific Rattlesnakes. Ann Emerg Med. 2002;40:619–624
  50. Glenn JL, Straight RC. Mojave rattlesnake Crotalus scutulatus scutulatus venom: variation in toxicity with geographical origin. Toxicon. 1978;16:81–84
  51. Rael ED, Johnson JD, Molina O, McCrystal HK. Distribution of Mojave toxin-like protein in rock rattlesnake (Crotalus lepidus) venom. In:  Campbell JA,  Brodie ED editor. Biology of the Pitvipers. Tyler, TX: Selva Press; 1992;p. 163–168
  52. Pinho FMO, Zanetta DMT, Burdmann EA. Acute renal failure after Crotalus durissus snakebite: a prospective survey on 100 patients. Kidney Int. 2005;67:659–667
  53. Flegal KM, Carroll MD, Ogden CL, Johnson CL. Prevalence and trends in obesity among US adults, 1999-2000. JAMA. 2002;288:1723–1727
  54. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM. Prevalence of overweight and obesity in the United States, 1999-2004. JAMA. 2006;295:1549–1555
  55. Guh DP, Zhang W, Bansback N, Amarsi Z, Birmingham CL, Anis AH. The incidence of co-morbidities related to obesity and overweight: a systematic review and meta-analysis. BMC Public Health. 2009;9:88
  56. Curry SC, Horning D, Brady P, Requia R, Kunkel DB, Vance MV. The legitimacy of rattlesnake bites in central Arizona. Ann Emerg Med. 1989;18:658–663
  57. Dart RC, McNally JT, Spaite DW, Gustafson R. The sequelae of pitviper poisoning in the United States. In:  Campbell JA,  Brodie ED editor. Biology of the Pitvipers. Tyler, TX: Selva Press; 1992;p. 395–404
  58. Morandi N, Williams J. Snakebite injuries: contributing factors and intentionality of exposure. Wilderness Environ Med. 1997;8:152–155
  59. LoVecchio F, DeBus DM. Snakebite envenomation in children: a 10-year retrospective review. Wilderness Environ Med. 2001;12:184–189
  60. Tanen DA, Ruha A-M, Graeme KA, Curry SC. Epidemiology and hospital course of rattlesnake envenomations cared for at a tertiary referral center in central Arizona. Acad Emerg Med. 2001;8:177–182
  61. Matteucci MJ, Hannum JE, Riffenburgh RH, Clark RF. Pediatric sex group differences in location of snakebite injuries requiring antivenom therapy. J Med Toxicol. 2007;3:103–106
  62. Pizon AF, Riley BD, LoVecchio F, Gill R. Safety and efficacy of Crotalidae polyvalent immune Fab in pediatric crotaline envenomations. Acad Emerg Med. 2007;14:373–376
  63. Campbell BT, Corsi JM, Boneti C, Jackson RJ, Smith SD, Kokoska ER. Pediatric snakebites: lessons learned from 114 cases. J Pediatr Surg. 2008;43:1338–1341
  64. Sotelo N. Review of treatment and complications in 79 children with rattlesnake bite. Clin Pediatr (Phila). 2008;47:483–489
  65. Moss ST, Bogdan G, Dart RC, Nordt SP, Williams SR, Clark RF. Association of rattlesnake bite location with severity of clinical manifestations. Ann Emerg Med. 1997;30:58–61
  66. Redd SC. Asthma in the United States: burden and current theories. Environ Health Perspect. 2002;110(suppl 4):557–560
  67. Corbett SW. Asthma exacerbations during Santa Ana winds in southern California. Wilderness Environ Med. 1996;4:304–311
  68. Meng Y-Y, Wilhelm M, Rull RP, English P, Ritz B. Traffic and outdoor air pollution levels near residences and poorly controlled asthma in adults. Ann Allergy Asthma Immunol. 2007;98:455–463
  69. Künzli N, Bridevaux PO, Liu S, et al. Traffic-related air pollution correlates with adult-onset asthma among never-smokers. Thorax. 2009;64:664–670
  70. Lounsbery MG, Bubak ME. The impact of secondhand smoke on children: respiratory and other medical concerns. South Dakota Med. 2009;Spec No:13–16
  71. Van Dole KB, Swern AS, Newcomb K, Nelsen L. Seasonal patterns in health care use and pharmaceutical claims for asthma prescriptions for preschool- and school-aged children. Ann Allergy Asthma Immunol. 2009;102:198–204
  72. Vlaski E, Stavric K, Seckova L, Kimovska M, Isjanovska R. Influence of physical activity and television-watching time on asthma and allergic rhinitis among young adolescents: preventive or aggravating?. Allergol Immunopathol (Madr). 2008;36:247–253
  73. Parsons JP, Mastronarde JG. Exercise-induced asthma. Curr Opin Pulm Med. 2009;15:25–28
  74. Lin RY, Cannon AG, Teitel AD. Pattern of hospitalizations for angioedema in New York between 1990 and 2003. Ann Allergy Asthma Immunol. 2005;95:159–166
  75. Lin RY, Anderson AS, Shah SN, Nurruzzaman F. Increasing anaphylaxis hospitalizations in the first 2 decades of life: New York State, 1990–2006. Ann Allergy Asthma Immunol. 2008;101:387–393
  76. Benítez JA, Rifakis PM, Vargas JA, Cabaniel G, Rodríguez-Morales AJ. Trends in fatal snakebites in Venezuela, 1995-2002. Wilderness Environ Med. 2007;18:209–213
  77. Ribeiro LA, Gadia R, Jorge MT. Comparison between the epidemiology of accidents and the clinical features of envenoming by snakes of the genus Bothrops, among elderly and non-elderly adults. Rev Soc Bras Med Trop. 2008;41:46–49
  78. State of Arizona, Office of the Governor. Aging 2020: Arizona's Plan for an Aging Population. Phoenix, AZ: Office of the Governor http://www.azgovernor.gov/Aging/Documents/Aging2020Report.pdfAccessed May 17, 2009
  79. Brice AJ. Access to health service delivery for Hispanics: a communication issue. Multicult Nurs Health. 2000;6:7–17
  80. Garza A, Rodriguez-Lainz A, Ornelas IJ. The health of the California region bordering Mexico. J Immigr Health. 2004;6:137–144
  81. Dart RC, McNally J. Efficacy, safety, and use of snake antivenoms in the United States. Ann Emerg Med. 2001;37:181–188
  82. Norris RL, Thompson RC, Dery R, et al. Regional versus systemic antivenom administration in the treatment of snake venom poisoning in a rabbit model: a pilot study. Wilderness Environ Med. 2003;14:231–235
  83. Brooks DE, Graeme KA, Ruha AM, Tanen DA. Respiratory compromise in patients with rattlesnake envenomation. J Emerg Med. 2002;23:329–332
  84. Brooks DE, Graeme KA. Airway compromise after first rattlesnake envenomation. Wilderness Environ Med. 2004;15:188–193
  85. Offerman SR, Smith TS, Derlet RW. Does the aggressive use of polyvalent antivenin for rattlesnake bites result in serious acute side effects?. West J Med. 2001;175:88–91
  86. Cannon R, Ruha A-M, Kashani J. Acute hypersensitivity reactions associated with administration of Crotalidae polyvalent immune Fab antivenom. Ann Emerg Med. 2008;51:407–411
  87. Isbister GK, Brown SG, MacDonald E, White J, Currie BJ. Current use of Australian snake antivenoms and frequency of immediate-type hypersensitivity reactions and anaphylaxis. Med J Aust. 2008;188:473–476
  88. de Medeiros CR, Barbaro KC, Lira MS, et al. Predictors of Bothrops jararaca venom allergy in snake handlers and snake venom handlers. Toxicon. 2008;51:672–680
  89. Gold BS, Dart RC, Barish RA. Bites of venomous snakes. N Engl J Med. 2002;347:347–356
  90. Tokish JT, Benjamin J, Walter F. Crotalid envenomation: the southern Arizona experience. J Orthop Trauma. 2001;15:5–9
  91. Seger D, Kahn S, Krenzelok EP. Treatment of US Crotalidae bites: comparisons of serum and globulin-based polyvalent and antigen-binding fragment antivenins. Toxicol Rev. 2005;24:217–227
  92. Munekiyo SM, Mackessy SP. Effects of temperature and storage conditions on the electrophoretic, toxic and enzymatic stability of venom components. Comp Biochem Physiol. 1998;119B:119–127
  93. Munekiyo SM, Mackessy SP. Presence of peptide inhibitors in rattlesnake venoms and their effects on endogenous metalloproteases. Toxicon. 2005;45:255–263
  94. Mackessy SP, Baxter LM. Bioweapons synthesis and storage: the venom gland of front-fanged snakes. Zool Anz. 2006;245:147–159
  95. Adams CE, Thomas JK. Texas Rattlesnake Roundups. College Station, TX: Texas A&M University Press; 2008;
  96. Parks CM, Toth JP. Fluency, familiarity, aging, and the illusion of truth. Aging Neuropsychol Cogn. 2006;13:225–253
  97. O'Neil ME, Mack KA, Gilchrist J, Wozniak EJ. Snakebite injuries treated in United States emergency departments, 2001–2004. Wilderness Environ Med. 2007;18:281–292
  98. Gutiérrez JM, Theakston RD, Warrell DA. Confronting the neglected problem of snake bite envenoming: the need for a global partnership. PLoS Med. 2006;3:e150
  99. Kasturiratne A, Wickremasinghe AR, de Silva N, et al. The global burden of snakebite: a literature analysis and modelling based on regional estimates of envenoming and deaths. PLoS Med. 2008;5:e218
  100. Chippaux JP. Snakebite in Africa: current situation and urgent needs. In:  Mackessy SP editors. Handbook of Venoms and Toxins of Reptiles. Boca Raton, FL: Taylor & Francis/CRC Press; 2009;p. 453–473
  101. Simpson ID, Norris RL. The global snakebite crisis—a public health issue misunderstood, not neglected. Wilderness Environ Med. 2009;20:43–56
  102. Doley R, Mackessy SP, Kini RM. Role of accelerated segment switch in exons to alter targeting (ASSET) in the molecular evolution of snake venom proteins. BMC Evol Biol. 2009;9:146
  103. Beaman KR, Hayes WK. Rattlesnakes: research trends and annotated checklist. In:  Hayes WK,  Beaman KR,  Cardwell MD,  Bush SP editor. The Biology of Rattlesnakes. Loma Linda, CA: Loma Linda University Press; 2008;p. 5–16
  104. Parrish HM, Goldner JC, Silberg SL. Comparison between snakebites in children and adults. Pediatrics. 1965;36:251–256

PII: S1080-6032(10)00060-8

doi: 10.1016/j.wem.2010.01.006

Wilderness & Environmental Medicine
Volume 21, Issue 1 , Pages 35-45 , March 2010