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Berezina D.I., Fomina L.L., Kulakova T.S., Tkacheva E.S., Popova V.V. Comparing the influence of temperature on the coagulation activity of blood plasma in vitro in poikilothermic and home-othermic animals. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2025, Vol. 60, № 4, p. 681-697.
(how to cite this article)

doi: 10.15389/agrobiology.2025.4.681eng

UDC: 636:612.115:57.089

Acknowledgements:
Supported financially by the Russian Science Foundation, no. 23-26-00115, https://rscf.ru/project/23-26-00115/

 

COMPARING THE INFLUENCE OF TEMPERATURE ON THE COAGULATION ACTIVITY OF BLOOD PLASMA in vitro IN POIKILOTHERMIC AND HOMEOTHERMIC ANIMALS

D.I. Berezina1 ✉, L.L. Fomina2, T.S. Kulakova2,
E.S. Tkacheva2, V.V. Popova3

1PE Didenko T.V., 2А, ul. Marshala Koneva, Vologda, 160000 Russia, e-mail vetxwork@gmail.com (✉ corresponding author);
2Vereshchagin Vologda SDFA, 2, ul, Shmidta, Molochnoe, Vologda, 160555 Russia, e-mail fomina.l.l@2.molochnoe.ru, dofas@yandex.ru, elfenia@mail.ru;
3LLC Aquaculture, 5/4н, ul. Metallurgov, Cherepovets, Vologda Province, 162606 Russia, e-mail pvv@tdak.ru

ORCID:
Berezina D.I. orcid.org/0000-0002-5243-7808
Tkacheva E.S. orcid.org/0000-0003-3651-5359
Fomina L.L. orcid.org/0000-0001-6850-6663
Popova V.V. orcid.org/0009-0002-0143-1227
Kulakova T.S. orcid.org/0000-0001-6247-4699

Final revision received September 30, 2024
Accepted October 22, 2024

Hemostasis is a physiological process that is well-controlled and complex in the body that ensures the optimal state of blood aggregation. Deviations from the optimal temperature for the interaction between the various coagulation enzymes greatly affect the fine biochemistry of coagulation and anticoagulation processes. In vitro studies of thermal effects on the coagulation profile of animals contribute to the study of various features and pathologies of hemostasis that lead to animal diseases. The study of animal blood coagulation activity at different temperatures is crucial for human medicine, as coagulopathies are studied in animal models with body temperatures that differ from human ones. For the first time, changes in the activity of various coagulation cascade pathways (secondary hemostasis) were determined in cold-blooded (African sharptooth catfish, common carp, rainbow trout) and warm-blooded (chicken, cattle) animals under temperature conditions modulating hypo-, normal-, and hyperthermia in vitro. The aim of this study was to evaluate the differences in hemostasis parameters between animals with different thermobiological status when plasma incubation temperature changes in vitro are influenced. The study was conducted in Vologda SDFA in 2023. Healthy rainbow trout (Oncorhynchus mykiss W., n = 15), African sharptooth catfish (Clarias gariepinus B., n = 10), and common carp (Cyprinus carpio L., n = 15) were used as poikilothermic (cold-blooded) animals. Healthy Ayrshire cows (Bos taurus L., n = 15) at different stages of lactation, 4-6 years old, and healthy hens (Gallus gallus L., n = 19) of the Rhode Island Red breed 2 years old were studied as homoiothermic (warm-blooded) animals. Blood samples were collected in IMPROVACUTER tubes (Guangzhou Improve Medical Instruments Co., Ltd, China) containing 3.8 % sodium citrate solution in a 1:9 ratio. Prior to blood collection, the fish were anesthetized by introducing clove oil into the water at a concentration of 0.033 ml/l and maintaining them in this solution for 15 minutes. Subsequently, samples were obtained through puncture of the caudal hemal canal. In birds, blood was obtained by puncture of the axillary vein, in cattle by puncture of the caudal vein. Platelet-poor plasma was obtained by centrifugation of blood in a CM-6M centrifuge (ELMI laboratory technology, Ltd, Latvia) at 3000 rpm for 20 min. The state of plasma-coagulation hemostasis was evaluated using indicators such as APTT (Activated partial thromboplastin time), PT (Prothrombin time), TT (Thrombin time) and analysis of fibrinogen activity automatically using a coagulometer Thrombostat (Behnk Elektronik GmbH & Co., Germany) at 37 °C, and manually using a medical water thermostat TW-2 (ELMI laboratory technology, Ltd, Latvia) temperatures of 46 °C, 43 °C, 40 °C, 28 °C, 24 °C and 18 °C. The anticoagulation properties of blood were assessed by assessing the activity of Antithrombin III in blood plasma at the same temperatures. The research employed reagents produced by Tekhnologiya-Standart LLC (Russia) and NPO RENAM (Russia). Statistical analysis has shown that when heated in vitro, the coagulation system of warm-blooded animals exhibits a tendency towards hypercoagulation, which can vary depending on the coagulation mechanisms involved. In the case of cattle, there is a significant activation of the coagulation process through tissue factors and a decrease in the effectiveness of anticoagulant mechanisms, namely PT (R = -0.79; p ≤ 0.01) and antithrombin activity (R = -0.8; p ≤ 0,01) are 60% reliable dependent on the temperature of the reaction medium. Birds demonstrate increased coagulation along the common pathway (R = -0.8; p≤0.01) with a simultaneous decrease in fibrinogen activity (R = -0.8; p ≤ 0.01), the proportion of the influence of temperature in which are approx. 71 % and 39 %,, respectively. Fish and other poikilothermic animals reliably confirm a diverse thermally-mediated hemostasis response. Carp was characterized by hypocoagulation by reducing tissue activation of coagulation, where the PT value (R = 0.8; p ≤ 0.01) was 50 % determined by the plasma incubation temperature. Catfish showed a significant array of hypercoagulation processes, resulting from a rise in fibrinogen activity (R = -0.7; p ≤ 0.01) and a decrease in antithrombin activity (R = -0.8; p ≤ 0.01). Among all fish species studied, catfish has the plasma blood coagulation factors that are the most thermolabile or species-specific. There were no significant relationships established for trout. The thermal regime in standard humane medicine coagulological studies has been shown to affect the activation of blood coagulation in animals in vitro, but the changes are not specific to poikilotermic and homoerothermic. The data obtained can be used to develop coagulological tests adapted for biology, zoology and veterinary science. The observed patterns will contribute to a deeper understanding of the thermal stability of the animal body and the development of biomarkers for thermal stress.

Keywords: hemostasis, blood, temperature, cattle, bird, fish.

 

REFERENCES

  1. Sejian V., Bhatta R., Gaughan J.B., Dunshea F.R., Lacetera N. Review: Adaptation of animals to heat stress. Animal, 2018, 12(Suppl. 2): s431-s444 CrossRef
  2. Versteeg H.H., Heemskerk J.W., Levi M., Reitsma P.H. New fundamentals in hemostasis. Physiological Reviews, 2013, 93(1): 327-358 CrossRef
  3. Stassen J.M., Arnout J., Deckmyn H. The hemostatic system.Current Medicinal Chemistry, 2004, 11(17): 2245-2260 CrossRef
  4. Doolittle R.F. The evolution of vertebrate blood coagulation: a case of Yin and Yang. Thrombosis and Haemostasis, 1993, 70(01): 024-028 CrossRef
  5. Doolittle R.F., Surgenor D.M. Blood coagulation in fish. American Journal of Physiology-Legacy Content, 1962, 203(5): 964-970 CrossRef
  6. Doerr J.A., Hamilton P.B. New evidence for intrinsic blood coagulation in chickens. Poultry Science, 1981, 60(1): 237-242 CrossRef
  7. Sturkie P.D. Avian physiology. Springer Science & Business Media, NY, 2012.
  8. Doolittle R.F. Step-by-step evolution of vertebrate blood coagulation. Cold Spring Harbor Symposia on Quantitative Biology, 2009, 74: 35-40 CrossRef
  9. Maden M., Yildiz R., Çöl R., Arican M., Ider M., Garip M., Tras B. The evaluation of hemostatic dysfunctionand disseminated intravascular coagulationin dairy cows with abomasal displacement. Polish Journal of Veterinary Sciences, 2018, 21(4): 769-778 CrossRef
  10. Reck Jr. J., Berger M., Terra R.M.S., Marks F.S., da Silva Vaz Jr. I., Guimarães J.A., Termignoni C. Systemic alterations of bovine hemostasis due to Rhipicephalus (Boophilus) microplus infestation. Research in Veterinary Science, 2009, 86(1): 56-62 CrossRef
  11. Bobowiec R., Wessely-Szponder J., Hola P. Crosstalk between coagulation and inflammation in mastitis and metritis in dairy cows. Acta Veterinaria Hungarica, 2009, 57(2): 283-293 CrossRef
  12. Berezina D.I., Fomina L.L., Goreva A.D. Effect of stress factors on the coagulogram of common carp, Cyprinus carpio. Biosciences Biotechnology Research Asia, 2020, 17(3): 629-635 CrossRef
  13. Rodenbaugh C.I., Lyon S.D., Hanzlicek A.S., Kanda I., Payton M.E., Rizzi T.E., Holland L.A., Brandão J. Dynamic viscoelastic coagulometry of blood obtained from healthy chickens. American Journal of Veterinary Research, 2019, 80(5): 441-448 CrossRef
  14. Russell K.E., Heatley J.J. Avian hemostasis. In: Schalm's Veterinary Hematology. Seventh Edition. M.B. Brooks, K.E. Harr, D.M. Seelig, K.J. Wardrop, D.J. Weiss (eds.). John Wiley & Sons, Inc., 2022, 865-874 CrossRef
  15. Buzala M., Słomka A., Janicki B., Ponczek M.B., Żekanowska E. The mechanism of blood coagulation, its disorders and measurement in poultry. Livestock Science, 2017, 195: 1-8 CrossRef
  16. Schurgers E., Moorlag M., Hemker C., Lindhout T., Kelchtermans H., de Laat B. Thrombin generation in zebrafish blood. PLoS ONE, 2016, 11(2): e0149135 CrossRef
  17. Gruzdeva O.V., Bichkova E.E., Penskaya T.Yu., Kuz’mina A.A., Antonova L.V., Barbarash L.S. Sovremennie tekhnologii v meditsine, 2021, 13(1): 52-58 CrossRef (in Russ.).
  18. Gong P., Zhang M.-Y., Zhao H., Tang Z.R., Hua R., Mei X., Cui J., Li C.S. Effect of mild hypothermia on the coagulation-fibrinolysis system and physiological anticoagulants after cardiopulmonary resuscitation in a porcine model. PloS ONE, 2013, 8(6): e67476 CrossRef
  19. Bouchama A., Roberts G., Al Mohanna F., El-Sayed R., Lach B., Chollet-Martin S., Ollivier V., Al Baradei R., Loualich A., Nakeeb S., Eldali A., de Prost D. Inflammatory, hemostatic, and clinical changes in a baboon experimental model for heatstroke. Journal of Applied Physiology, 2005, 98(2): 697-705 CrossRef
  20. Brooks M.B., Stokol T., Catalfamo J.L. Comparative hemostasis: animal models and new hemostasis tests. Clinics in Laboratory Medicine, 2011, 31(1): 139-159 CrossRef
  21. Suvernev A.V., Ivanov G.V. Intensivnoe teplolechenie [Intensive heat therapy]. Novosibirsk, 2014 (in Russ.).
  22. Ivanov A.A. Fiziologiya rib: uchebnoe posobie [Fish physiology: a textbook]. St. Petersburg, 2021 (in Russ.).
  23. Levi M. Hemostasis and thrombosis in extreme temperatures (hypo-and hyperthermia). Seminars in Thrombosis and Hemostasis, 44(07): 651-655 CrossRef
  24. Evans D.H., Claiborne J.B., Currie S. The physiology of fishes. CRC Press, FL, 2023.
  25. Botyazhova O.A. Fiziologiya sistemi krovi: sravnitel’nie, ekologicheskie i evolyutsionnie aspekti: uchebnoe posobie [Physiology of the blood system: comparative, ecological and evolutionary aspects: a textbook]. Yaroslavl’, 2000 (in Russ.).
  26. Tavares-Dias M., Oliveira S.R. A review of the blood coagulation system of fish. Revista Brasileira de Biociências, 2009, 7(2): 205-224.
  27. Basu N., Todgham A.E., Ackerman P.A., Bibeau M.R., Nakano K., Schulte P.M., Iwama G. K. Heat shock protein genes and their functional significance in fish.Gene,2002, 295(2): 173-183 CrossRef
  28. Xie S., Tearle R., McWhorter T.J. Heat shock protein expression is upregulated after acute heat exposure in three species of Australian desert birds. Avian Biology Research, 2018, 11(4): 263-273 CrossRef
  29. Van Pittius M.G., Van Vuren J.H., Du Preez H.H. Effects of chromium during pH change on blood coagulation in Tilapia sparrmanii (Cichlidae). Comparative Biochemistry and Physiology: C, Comparative Pharmacology and Toxicology,1992, 101(2): 371-374 CrossRef
  30. Nikolaev V.Yu. Sostoyanie sistemi gemostaza pri obshchem peregrevanii u kris. Kandidatskaya dissertatsiya [The state of the hemostasis system during general overheating in rats. PhD Thesis]. Barnaul, 2016 (in Russ.).
  31. Wu J., Yuan W., Li J., Zhao Y., Li J., Li Z., Li C. Effects of mild hypothermia on cerebral large and small microvessels blood flow in a porcine model of cardiac arrest.Neurocritical Care, 2017, 27: 297-303 CrossRef
  32. Münster A.M.B., Olsen A.K., Bladbjerg E.M. Usefulness of human coagulation and fibrinolysis assays in domestic pigs. Comparative Medicine, 2002, 52(1): 39-43.
  33. Hamackova J., Kouril J., Kozak P., Stupka Z. Clove oil as an anaesthetic for different freshwater fish species. Bulgarian Journal of Agricultural Science, 2006, 12(2): 185-194.
  34. Shikhova O.A. Matematicheskaya biostatistika: Metodicheskie ukazaniya i individual’nie zadaniya [Mathematical biostatistics: methodical instructions and individual assignments]. Vologda—Molochnoe, 2017 (in Russ.).
  35. Berezina D.I., Fomina L.L., Kulakova T.S., Modanova K.E., Popova V.V. Effect of temperature on the coagulation activity of blood plasma in rainbow trout (Oncorhynchus Mykiss), common carp(Cyprinus Carpio), and North African Catfish (Clarias Gariepinus) in vitro. Inland Water Biology, 2024, 17(5): 853-862 CrossRef
  36. Cheng M., McCarl B., Fei C. Climate change and livestock production: a literature review. Atmosphere, 2022, 13(1): 140 CrossRef
  37. Min L., Cheng J., Zhao S., Tian H., Zhang Y., Li S., Yang H., Zheng N., Wang J. Plasma-based proteomics reveals immune response, complement and coagulation cascades pathway shifts in heat-stressed lactating dairy cows. Journal of Proteomics, 2016, 146: 99-108 CrossRef
  38. Burhans W.S., Burhans C.R., Baumgard L.H. Invited review: Lethal heat stress: The putative pathophysiology of a deadly disorder in dairy cattle. Journal of Dairy Science, 2022, 105(5): 3716-3735 CrossRef
  39. Gómez-Prado J., Pereira A.M., Wang D., Villanueva-García D., Domínguez-Oliva A., Mora-Medina P., Hernández-Avalos I., Martínez-Burnes J., Casas-Alvarado A., Olmos-Hernández A., Ramírez-Necoechea R., Verduzco-Mendoza A., Hernández A., Torres F., Mota-Rojas D. Thermoregulation mechanisms and perspectives for validating thermal windows in pigs with hypothermia and hyperthermia: an overview. Frontiers in Veterinary Science, 2022, 9: 74-94 CrossRef
  40. Zaragoza O.D.R., Rodríguez M.H., Bückle Ramirez L.F. Thermal stress effect on tilapia Oreochromis mossambicus (Pisces: Cichlidae) blood parameter. Marine and Freshwater Behaviour and Physiology, 2008, 41(2): 79-89 CrossRef
  41. Ruis M.A.W., Bayne C.J. Effects of acute stress on blood clotting and yeast killing by phagocytes of rainbow trout. Journal of Aquatic Animal Health, 1997, 9(3): 190-195 CrossRef
  42. Diehl K.A., Crawford E., Shinko P.D., Tallman Jr R.D., Oglesbee M.J. Alterations in hemostasis associated with hyperthermia in a canine model. American Journal of Hematology, 2000, 64(4): 262-270 CrossRef
  43. Moskalenko S.V., Shakhmatov I.I., Kiselёv V.I., Nikolaev V.Yu. Mezhdunarodniy zhurnal prikladnikh i fundamental’nikh issledovaniy, 2015, 11(3): 36-365 (in Russ.).
  44. Feeney R.E., Vandenheede J., Osuga D.T. Macromolecules from cold-adapted antarctic fishes. Die Naturwissenschaften, 1972, 59(1): 22-29 CrossRef
  45. Langdell R.D., Bryan F.T., Gibson Jr. W.S. Coagulation of catfish blood. Proceedings of the Society for Experimental Biology and Medicine, 1965, 118(2): 439-441.
  46. Kawatsu H. Clotting time of common carp blood. Bull. Japanese Soc. Sci. Fish, 1986, 52(4): 591-595 CrossRef
  47. Licheva N.A., Shakhmatov I.I., Kiselev V.I. Byulleten’ sibirskoy meditsini, 2017, 16(1): 50-58 CrossRef (in Russ.).
  48. Yoshihara H., Yamamoto T., Mihara H. Changes in coagulation and fibrinolysis occurring in dogs during hypothermia. Thrombosis Research, 1985, 37(4): 503-512 CrossRef
  49. Hessel II E.A., Schmer G., Dillard D.H. Platelet kinetics during deep hypothermia. Journal of Surgical Research, 1980, 28(1): 23-34 CrossRef
  50. Storey K.B. Out cold: biochemical regulation of mammalian hibernation—a mini-review. Gerontology, 2010, 56(2): 220-230 CrossRef
  51. Berkovskiy A.L., Sergeeva E.V., Suvorov A.V. Veterinariya, 2018, 5: 54-57 (in Russ.).
  52. Burke A., Reems M., Spriggs, M. Point‐of‐care viscoelastic coagulation monitor parameters in Amazon parrots (Amazona spp.). Journal of Veterinary Emergency and Critical Care, 2024, 34(3): 238-244 CrossRef
  53. Keller K.A., Guzman D.S.M., Acierno M.J., Beaufrère H., Sinclair K.M., Owens S.D., Paul-Murphy J., Tully T.N. Thromboelastography values in Hispaniolan Amazon parrots (Amazona ventralis): a pilot study. Journal of Avian Medicine and Surgery, 2015, 29(3): 174-180 CrossRef
  54. Kheirabadi B.S., Delgado A.V., Dubick M.A., Scherer M. R., Fedyk C. G., Holcomb J. B., Pusateri A.E. In vitro effect of activated recombinant factor VII (rFVIIa) on coagulation properties of human blood at hypothermic temperatures. Journal of Trauma and Acute Care Surgery, 2007, 63(5): 1079-1086 CrossRef
  55. Lewis J.H. Comparative hemostasis in vertebrates. USA, NY, Springer Science & Business Media, 1996.
  56. Guddorf V., Rohn K., Kummerfeld N., Mischke R. Comparative aspects of blood coagulation measurements in various wild and captive bird species. Tierärztliche Praxis Ausgabe K: Kleintiere/Heimtiere, 2017, 45(04): 246-252 CrossRef
  57. Klainbart S., Agi L., Bdolah-Abram T., Kelmer E., Aroch I. Clinical, laboratory, and hemostatic findings in cats with naturally occurring sepsis. Journal of the American Veterinary Medical Association, 2017, 251(9): 1025-1034 CrossRef
  58. Barthélemy A., Magnin M., Pouzot‐Nevoret C., Bonnet‐Garin J. M., Hugonnard M., Goy‐Thollot I. Hemorrhagic, hemostatic, and thromboelastometric disorders in 35 dogs with a clinical diagnosis of leptospirosis: a prospective study. Journal of Veterinary Internal Medicine, 2017? 31(1): 69-80 CrossRef
  59. Sobiech P., Radwińska J., Targoński R., Eleusizowa A., Tuyakova R., Żarczyńska K., Mitura A., Snarska A. Changes of the blood coagulation system of Holstein-Friesian heifers during the course of chlamydiosis. Vet. Arhiv, 2017, 87(1): 25-33.

 

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