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Hematological and biochemical reference intervals for Bothrops asper and Crotalus simus (Serpentes: Viperidae), maintained in captivity for venom extraction

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Abstract

This study presents hematological and biochemical reference intervals (RIs) for two species of viper snakes (Bothrops asper and Crotalus simus), which are the first of their type particularly for these two species maintained in captivity and for extraction of venom purposes. A total of 77 snakes were used in developing the study; specifically 39 B. asper and 38 C. simus snakes. Blood samples were obtained by puncturing the caudal vein, and hematological tests were performed manually by two independent technicians. Plasma biochemistry parameters were determined by an automatized analyzer. There are hematological differences between wild-caught and captive B. asper in the percentage of heterophils (P < 0.001), while in captive and wild-caught C. simus, the differences are found in the percentage of eosinophils, lymphocytes, and monocytes (P < 0.001). Differences in glucose (P = 0.012), uric acid (P < 0.001), and cholinesterase (P = 0.004) are found in captive and wild-caught B. asper. Differences in albumin (P = 0.002), calcium (P < 0.001), CK (P = 0.04), and LDH (P = 0.037) are found between captive and wild-caught C. simus. This study constitutes the first set of hematological and biochemical RIs for B. asper and C. simus maintained in captivity with the purpose of producing antivenom in Costa Rica. The establishment of comprehensive RIs for hematology and plasma biochemistry for these two species of snakes is useful for interpretation of blood test results, moreover, to serving as a reference for viper snakes used for research purposes.

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References

  • Alape-Girón A, Sanz L, Escolano J et al (2008) Snake venomics of the lancehead pitviper Bothrops asper: geographic, individual, and ontogenetic variations. J Proteome Res 7:3556–3571

    Article  PubMed  Google Scholar 

  • Alleman AR, Jacobson ER, Raskin RE (1999) Morphological, cytochemical staining and ultrastructural characteristics of blood cells from eastern diamondback rattlesnakes (Crotalus adamanteus). Am J Vet Res 60(4):507–514

    CAS  PubMed  Google Scholar 

  • Allender MC, Mitchell MA, Phillips CA, Gruszynski K, Beasly VR (2006) Hematology, plasma biochemistry, and antibodies to select viruses in wild-caught eastern massasauga rattlesnakes (Sistrurus catenatus catenatus) from Illinois. J Wildl Dis 42(1):107–114

    Article  PubMed  Google Scholar 

  • Ashley BD, Burchfield PM (1968) Maintenance of a snake colony for the purpose of venom extraction. Toxicon 5:267–275

    Article  CAS  PubMed  Google Scholar 

  • Bolaños F, Savage JM (2009) A checklist of the amphibian and reptiles of Costa Rica: additions and nomenclature revisions. Zootaxa 2005:1–23

    Google Scholar 

  • Braun JP, Concordet D, Geffré A, Abella NB, Trumel C (2013) Confidence intervals of reference limits in small reference sample groups. Vet Clin Pathol 42(3):395–398

    Article  CAS  PubMed  Google Scholar 

  • Brown GP, Shilton CM, Shine R (2006) Do parasites matter? Assessing the fitness consequences of haemogregarine infection in snakes. Can J Zool 84:668–676

    Article  Google Scholar 

  • Bryant GL, Fleming PA, Twomey L, Warren KA (2012) Factors affecting hematology and plasma biochemistry in the southwest carpet python (Morelia spilota imbricata). J Wildl Dis 48(2):282–294

    Article  CAS  PubMed  Google Scholar 

  • Burtis CA, Ashwood ER, Bruns DE (2008) Tietz fundamentals of clinical chemistry, 5th edn. Saunders, USA

    Google Scholar 

  • Campbell TW (2015) Exotic animal hematology and cytology. 4th ed. John Wiley & Sons, Inc. Wiley Blackwell, pp 67–83

  • Clark NB (1966) Influence of estrogens upon serum calcium, phosphate and protein concentration of fresh-water turtles. Comp Biochem Physiol 20:823–834

    Article  Google Scholar 

  • Dessauer HC (1970) Blood chemistry of reptiles: physiological and evolutionary aspects. Academic Press Inc, London

    Google Scholar 

  • Fernández P, Gutiérrez JM (2008) Mortality due to snakebite envenomation in Costa Rica (1993–2006). Toxicon 52:530–533

    Article  PubMed  Google Scholar 

  • Flint M, Morton JM, Limpus CJ, Patterson-Kane JC, Murray PJ, Mills PC (2010) Development and application of biochemical and haematological reference intervals to identify unhealthy green sea turtles (Chelonia mydas). Vet J 185:299–304

    Article  PubMed  Google Scholar 

  • Friedrichs KR, Harr KE, Freeman KP et al (2012) ASVCP reference interval guidelines: determination of de novo reference intervals in veterinary species and other related topics. Vet Clin Pathol 41(4):441–453, ISSN 0275–6382

    Article  PubMed  Google Scholar 

  • Geffré A, Friedrichs K, Harr K, Concordet D, Trumel C, Braun JP (2009) Reference values: a review. Vet Clin Pathol 38(3):288–298

    Article  PubMed  Google Scholar 

  • Gillet AK, Flint M, Hulse L, Hanger J, Mills PC (2015) Haematological and biochemical reference intervals for three species of hydrophiine sea snakes (Hydrophis curtus, H. elegans and H. peronii) in Australia. Vet J 204:275–281

    Article  Google Scholar 

  • Gutiérrez JM (2009) Snakebite envenomation in Central America. In: Mackessy SP (ed) Handbook of venom and toxins of reptiles. CRC Press, Boca Raton, pp 491–507

    Chapter  Google Scholar 

  • Gutiérrez JM, León G, Burnouf T (2011) Antivenoms for the treatment of snakebite envenomings: the road ahead. Biologicals. doi:10.1016/j.biologicals.2011.02.005

    Google Scholar 

  • Hattingh J, Willemse GT (1967) Hematological observations on the puff adder, Bitis arietans (Ophidia: Viperidae). Herpetologica 32(3):245–247

    Google Scholar 

  • Kasturiratne A, Wickremasinghe AR, de Silva N et al (2008) The global burden of snakebite: a literature analysis and modeling based on regional estimates of envenoming and deaths. PLoS Med 5:e218

    Article  PubMed  PubMed Central  Google Scholar 

  • Labocha MK, Schutz H, Hayes JP (2014) Which body condition is the best? Oikos 123:111–119

    Article  Google Scholar 

  • MacMahon JA, Hamer AH (1975) Hematology of the sidewinder (Crotalus cerastes). Comp Biochem Phys A 51A:53–58

    Article  Google Scholar 

  • Mader DR, Horvath CC, Paul-Murphy J (1985) The hematocrit and serum profile of the gopher snake (Pituophis melanoleucus catenifer). J Zool Anim Med 16(4):139–140

    Article  Google Scholar 

  • Madsen T, Ujvari B, Olsson M (2005) Old pythons stay fit: effects of haematozoan infections on life history traits of a large tropical predator. Oecologia 142:407–412

    Article  PubMed  Google Scholar 

  • McDaniel RC, Grunow WA, Daly JJ, Plummer MV (1984) Serum chemistry of the diamond-backed water snake (Nerodia rhombifera rhombifera) in Arkansas. J Wildl Dis 20(1):44–46

    Article  CAS  PubMed  Google Scholar 

  • Murphy JB, Armstrong BL (1978) Maintenance of rattlesnake in captivity. University of Kansas, Lawrence

    Book  Google Scholar 

  • Parida SP, Dutta SK, Pal A (2014) Hematology and plasma biochemistry of wild-caught Indian cobra Naja (Linnaeus, 1758). J Venomous Anim Toxins Incl Trop Dis 20:14

    Article  Google Scholar 

  • Peig J, Green AJ (2009) New perspective for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891

    Article  Google Scholar 

  • Salakij C, Salakij J, Apibal S, Narkkong NA, Chanhome L, Rochanapat N (2002) Hematology, morphology, cytochemical staining, and ultrastructural characteristics of blood cells in king cobras (Ophiophagus hannah). Vet Clin Pathol 31(3):116–126

    Article  PubMed  Google Scholar 

  • Sanchez-Hernandez JC (2003) Evaluating reptile exposure to cholinesterase-inhibiting agrochemicals by serum butyrylcholinesterase activity. Environ Toxicol Chem 22(2):296–301

    Article  CAS  PubMed  Google Scholar 

  • Savage JM (2002) The amphibians and reptiles of Costa Rica: a Herpetofauna between two continents, and two seas. The University of Chicago Press, Chicago

    Google Scholar 

  • Strum KM, Alfaro M, Haase B et al (2008) Plasma cholinesterases for monitoring pesticide exposure in nearctic-neotropical migratory shorebirds. Ornitologia Neotropical 19:1–11

    Google Scholar 

  • Thrall MA, Baker DC, Campbell TW et al (2006) Veterinary hematology and chemical chemistry. Blackwell Publishing, pp 259–276; 493–498

  • Troiano JC, Vidal JC, Gould J, Gould E (1997) Haematological reference intervals of the South American rattlesnake (Crotalus durissus terrificus, Laurenti, 1768) in captivity. Comp Haematol Int 1:109–112

    Article  Google Scholar 

  • Troiano JC, Vidal JC, Gould EF et al (1999) Haematology and blood chemical values from Bothrops ammodytoides (Ophidia-Crotalidae) in captivity. Comp Haematol Int 9:31–35

    Article  Google Scholar 

  • Troiano JC, Gould EG, Althaus R et al (2001) Blood chemical profile of the South American rattlesnake (Crotalus durissus terrificus) in captivity. J Venomous Anim Toxins 7(2):183–189

    Google Scholar 

  • Vasaruchapong T, Disarapong P, Chulasugandha P et al (2013) Comparative studies on hematological and plasma biochemical parameters in different types of venomous snakes in Thailand. Comp Clin Pathol. doi:10.1007/s00580-013-1721-9

    Google Scholar 

  • Wack RF, Hansen E, Small M, Poppenga R, Bunn D, Johnson CK (2012) Hematology and plasma biochemistry values for the giant garter snake (Thamnophis gigas) and valley garter snake (Thamnophis sirtalis fitchi) in the central valley of California. J Wildl Dis 48(2):307–313

    Article  CAS  PubMed  Google Scholar 

  • WHO (2010) WHO guidelines for the production, control and regulation of snake antivenom immunoglobulins. World Health Organization, Geneva

    Google Scholar 

Download references

Acknowledgments

The authors thank the continuous support of JM Gutiérrez, Y. Angulo, and G. León on the development of this work. This work was performed in partial fulfillment of the Master degree of A. Gomez at the University of Costa Rica.

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Authors and Affiliations

  1. Serpentario, Instituto Clodomiro Picado, Facultad de Microbiología, Universidad de Costa Rica, San José, Costa Rica

    Aarón Gómez, Danilo Chacón & Santos Rodríguez

  2. Departamento de Análisis Clínicos, Facultad de Microbiología, Universidad de Costa Rica, San José, Costa Rica

    Cynthia Arroyo, Wilson Astorga & Manuel Jiménez

Authors
  1. Aarón Gómez
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  2. Cynthia Arroyo
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  3. Wilson Astorga
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  4. Danilo Chacón
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  5. Santos Rodríguez
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  6. Manuel Jiménez
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Corresponding author

Correspondence to Aarón Gómez.

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Funding

This work was financially supported by the Vicerrectoría de Investigación, University of Costa Rica, project 430-B3-702.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable national and institutional guidelines for the care and use of animals were followed. This study was approved by the Institutional Committee for the Care and Use of Laboratory Animals (CICUA) of the University of Costa Rica (No. Resolution 124, session 28/06/2012).

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All the authors agree with the content of this manuscript and all have significantly contributed to the performance of the study and the preparation of the manuscript. All authors have approved the final version of this manuscript.

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Gómez, A., Arroyo, C., Astorga, W. et al. Hematological and biochemical reference intervals for Bothrops asper and Crotalus simus (Serpentes: Viperidae), maintained in captivity for venom extraction. Comp Clin Pathol 25, 615–623 (2016). https://doi.org/10.1007/s00580-016-2240-2

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  • DOI: https://doi.org/10.1007/s00580-016-2240-2

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