Near-Newtonian Blood Behavior – Is It Good to Be a Camel?
Abstract: From a certain level of exercise-intensity onward, hematocrit increases in horses, which brings more oxygen carriers into the bloodstream. Camels, however, when used in competitive racing could be even in need of iron supplementation and blood transfusions due to a severe reduction of their available hematocrit compared to their resting hematocrit. Since the extrinsic and intrinsic mechanical properties of camel erythrocytes (RBC) are so different compared to RBCs of other mammals, the question arises whether this observation might be a response to endurance exercise aiming at keeping the RBC count low. Rheometry indicated dromedary camel blood to behave almost Newtonian, which is unique amongst mammals. Shear thinning did increase with the hematocrit, but remained marginal compared to horses. As a result, camel whole blood viscosity (WBV) exceeded horse WBV at high shear rates, an effect, which was significantly augmented when the packed cell volume (PCV) was increased. Therefore, in camels any infusion of RBCs into the bloodstream can increase the cardiac work and the energy input into the endothelium more effectively, which should generate vascular remodeling in the long term. Yielding, however, was completely absent in camel blood, confirming low cohesion between its components at quasi-static flow. Camel blood remained a viscous liquid without a threshold even at unphysiologically high PCVs. This can help to washout lactate when camels start to dehydrate and might contribute to the sustained working ability of these animals. The subtle pseudoplastic behavior and the high viscosity contrast across the RBC membrane point to weak coupling between blood flow and red cell behavior. We predict that RBCs flow as separate entities and can show various types of motion, which can lead to friction instead of being collectively aligned to the flow direction. In comparison to horses, this behavior will become relevant at higher RBC counts in front of flow obstacles and possibly cause vascular remodeling if the PCV rises during strenuous exercise, a matter that should be avoided.
Publication Date: 2019-07-17 PubMed ID: 31379608PubMed Central: PMC6650724DOI: 10.3389/fphys.2019.00906Google Scholar: Lookup
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Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research examines the unique properties of camel blood compared to horse blood and the impact on exercise intensity and endurance. It suggests that camel blood behaves in a nearly Newtonian manner, which helps in withstanding dehydration and can contribute to the sustained working ability of camels.
Overview of Research
- The study began by examining how hematocrit levels increase during intense exercise in horses by adding more oxygen carriers to the bloodstream.
- In camels, the study found, such intense exercise could require iron and blood transfusions due to a significant reduction in available hematocrit levels compared to rest levels.
Differences in Camel and Horse RBCs
- The researchers found noticeable differences between the mechanical properties of camel erythrocytes (RBC) and those of other mammals, leading them to consider whether camels naturally keep their RBC count low in response to endurance exercise.
- Through rheometry, the study discovered that the blood of dromedary camels behaves almost Newtonian, a quality unique amongst mammals.
- Although shear thinning did increase with hematocrit levels, it remained insignificant compared to horses.
Impact of Hematocrit Levels on Cardiac Efficiency
- The research found that whole blood viscosity (WBV) in camels surpassed that in horses at high shear rates. This effect is significantly augmented when packed cell volume (PCV) is increased.
- In camels, any infusion of RBCs can effectively increase cardiac work and energy input into the endothelium, which could lead to long-term vascular remodeling.
- However, yielding was absent in camel blood, confirming low cohesion between its components.
PHysiological Adaptations in Camel Blood
- Camel blood remains a viscous liquid even at high PCVs, which helps excrete lactate when camels start to dehydrate and might contribute to the animal’s sustained working ability.
- The subtle pseudoplastic behavior and the high viscosity contrast across the RBC membrane suggest weak coupling between blood flow and red cell behavior.
- Camel RBCs flow separately and can exhibit various types of motion, which may cause friction instead of lining up in the direction of flow.
- In comparison to horses, this unique behavior could become interesting with higher RBC counts in front of flow obstacles and may cause vascular remodeling if the PCV rises during rigorous exercise.
Cite This Article
APA
Windberger U, Auer R, Seltenhammer M, Mach G, Skidmore JA.
(2019).
Near-Newtonian Blood Behavior – Is It Good to Be a Camel?
Front Physiol, 10, 906.
https://doi.org/10.3389/fphys.2019.00906 Publication
Researcher Affiliations
- Center for Biomedical Research, Medical University of Vienna, Vienna, Austria.
- Center for Biomedical Research, Medical University of Vienna, Vienna, Austria.
- Center for Forensic Medicine, Medical University of Vienna, Vienna, Austria.
- Center for Biomedical Research, Medical University of Vienna, Vienna, Austria.
- Camel Reproduction Center, Dubai, United Arab Emirates.
References
This article includes 103 references
- Abdo MS, Ali AM, Prentis PF. Fine structure of camel erythrocytes in relation to its functions.. Z Mikrosk Anat Forsch 1990;104(3):440-8.
- Abkarian M, Faivre M, Viallat A. Swinging of red blood cells under shear flow.. Phys Rev Lett 2007 May 4;98(18):188302.
- Abkarian M, Viallat A. Deformability of red blood cells. .
- Abrhaley A, Leta S. Medicinal value of camel milk and meat. J. Appl. Anim. Res. 46 552–558.
- Akbar SJ, Derksen FJ, Billah AM, Werney U. Exercise induced pulmonary haemorrhage in racing camels.. Vet Rec 1994 Dec 24-31;135(26):624-5.
- Al-Hakak Z M. A comparative study between the blood pictures of Iraqi camels infected with trypanosomiasis and the blood picture of the healthy Iraqi camels. J. Global Pharma. Technol. 9 196–205.
- Al-Quarawi A A, Mousa H M. Lipid concentrations in erythrocyte membranes in normal, starved, dehydrated and rehydrated camels (Camelus dromedarius), and in normal sheep (Ovis aries) and goats (Capra hircus). J. Arid Environ. 59 675–683.
- Auer R, Gleiss A, Windberger U. Towards a basic understanding of the properties of camel blood in response to exercise. Emir. J. Food Agric. 27 302–311.
- Bäumler H, Neu B, Mitlöhner R, Georgieva R, Meiselman HJ, Kiesewetter H. Electrophoretic and aggregation behavior of bovine, horse and human red blood cells in plasma and in polymer solutions.. Biorheology 2001;38(1):39-51.
- Baier D, Mueller T, Windberger U. Force spectroscopy on red blood cells of different species: a comparative approach. .
- Baskurt OK, Farley RA, Meiselman HJ. Erythrocyte aggregation tendency and cellular properties in horse, human, and rat: a comparative study.. Am J Physiol 1997 Dec;273(6):H2604-12.
- Betz T, Lenz M, Joanny JF, Sykes C. ATP-dependent mechanics of red blood cells.. Proc Natl Acad Sci U S A 2009 Sep 8;106(36):15320-5.
- Böning D, Maassen N, Pries A. The hematocrit paradox--how does blood doping really work?. Int J Sports Med 2011 Apr;32(4):242-6.
- Bogdanis GC. Effects of physical activity and inactivity on muscle fatigue.. Front Physiol 2012;3:142.
- Bretherton F B. the motion of rigid particles in a shear flow at low Reynolds number. J. Fluid. Mech. 14 284–304.
- Bruce LJ, Ghosh S, King MJ, Layton DM, Mawby WJ, Stewart GW, Oldenborg PA, Delaunay J, Tanner MJ. Absence of CD47 in protein 4.2-deficient hereditary spherocytosis in man: an interaction between the Rh complex and the band 3 complex.. Blood 2002 Sep 1;100(5):1878-85.
- Cecchi E, Giglioli C, Valente S, Lazzeri C, Gensini GF, Abbate R, Mannini L. Role of hemodynamic shear stress in cardiovascular disease.. Atherosclerosis 2011 Feb;214(2):249-56.
- Chu H, McKenna MM, Krump NA, Zheng S, Mendelsohn L, Thein SL, Garrett LJ, Bodine DM, Low PS. Reversible binding of hemoglobin to band 3 constitutes the molecular switch that mediates O2 regulation of erythrocyte properties.. Blood 2016 Dec 8;128(23):2708-2716.
- Cluer D, Henkel P, Saltin B. Adaptations to training in the racing camel.. Acta Physiol Scand Suppl 1994;617:78-86.
- Cohen WD, Sorokina Y, Sanchez I. Elliptical versus circular erythrocyte marginal bands: isolation, shape conversion, and mechanical properties.. Cell Motil Cytoskeleton 1998;40(3):238-48.
- Dahl KN, Parthasarathy R, Westhoff CM, Layton DM, Discher DE. Protein 4.2 is critical to CD47-membrane skeleton attachment in human red cells.. Blood 2004 Feb 1;103(3):1131-6.
- Dunstan R H, Macdonald M M, Marks A, Sparkes D L, Roberts T K. Alterations in red blood cell parameters, plasma amino acids, total cholesterol and fatty acids in Standardbred horses undergoing fitness training. Comp. Exerc. Physiol. 15 13–23.
- Dupire J, Socol M, Viallat A. Full dynamics of a red blood cell in shear flow.. Proc Natl Acad Sci U S A 2012 Dec 18;109(51):20808-13.
- Eitan A, Aloni B, Livne A. Unique properties of the camel erythrocyte membrane, II. Organization of membrane proteins.. Biochim Biophys Acta 1976 Apr 5;426(4):647-58.
- El-Sayed MS, Ali N, El-Sayed Ali Z. Haemorheology in exercise and training.. Sports Med 2005;35(8):649-70.
- Evans DL, Rose RJ, Knight PK, Cluer D, Manefield GW. Some physiological responses to incremental treadmill exercise in the racing camel.. Acta Physiol Scand Suppl 1994;617:33-9.
- Fedde MR, Wood SC. Rheological characteristics of horse blood: significance during exercise.. Respir Physiol 1993 Dec;94(3):323-35.
- Fedosov DA, Caswell B, Karniadakis GE. A multiscale red blood cell model with accurate mechanics, rheology, and dynamics.. Biophys J 2010 May 19;98(10):2215-25.
- Fedosov DA, Noguchi H, Gompper G. Multiscale modeling of blood flow: from single cells to blood rheology.. Biomech Model Mechanobiol 2014 Apr;13(2):239-58.
- Fischer TM, Korzeniewski R. Effects of shear rate and suspending medium viscosity on elongation of red cells tank-treading in shear flow.. Cytometry A 2011 Nov;79(11):946-51.
- Fischer TM, Stöhr-Lissen M, Schmid-Schönbein H. The red cell as a fluid droplet: tank tread-like motion of the human erythrocyte membrane in shear flow.. Science 1978 Nov 24;202(4370):894-6.
- Forsyth AM, Wan J, Ristenpart WD, Stone HA. The dynamic behavior of chemically "stiffened" red blood cells in microchannel flows.. Microvasc Res 2010 Jul;80(1):37-43.
- Gaehtgens P, Will G, Schmidt F. Comparative rheology of nucleated and non-nucleated red blood cells. II. Rheological properties of avian red cells suspensions in narrow capillaries.. Pflugers Arch 1981 Jun;390(3):283-7.
- Gardner K, Bennett G V. Recently identified erythrocyte membrane-skeletal proteins. .
- Gaughan J B. Which physiological adaptation allows camels to tolerate high heat load – and what more can we learn?. J. Camelid. Sci. 4 85–88.
- Gedde MM, Yang E, Huestis WH. Resolution of the paradox of red cell shape changes in low and high pH.. Biochim Biophys Acta 1999 Mar 4;1417(2):246-53.
- Geor RJ, Lund EM, Weiss DJ. Echinocytosis in horses: 54 cases (1990).. J Am Vet Med Assoc 1993 Mar 15;202(6):976-80.
- Goldsmith H, Marlow J. Flow behavior of erythrocytes. I. rotation and deformation in dilute suspensions. Proc. R. Soc. London Ser. B 182 351–384.
- Goniakowska-Witalińska L, Witaliński W. Evidence for a correlation between the number of marginal band microtubules and the size of vertebrate erthrocytes.. J Cell Sci 1976 Nov;22(2):397-401.
- Gov N, Zilman AG, Safran S. Cytoskeleton confinement and tension of red blood cell membranes.. Phys Rev Lett 2003 Jun 6;90(22):228101.
- Guerra-Shinohara EM, Barretto OC. The erythrocyte cytoskeleton protein 4.2 is not demonstrable in several mammalian species.. Braz J Med Biol Res 1999 Jun;32(6):683-7.
- Hinchcliff K W, Geor R J, Kaneps A J. Equine Exercise Physiology: The Science of Exercise in the Athletic Horse. New York, NY: Saunders.
- Hunter R J, Nicol S K. The dependence of plastic flow behavior of clay suspensions on surface properties. J. Colloid Interface Sci. 28 250–259.
- Israelachvili J N. Intermolecular and Surface Forces, 3rd Edn. Cambridge: Academic Press., 469–499.
- Keller S R, Skalak R. Motion of a tank-treading ellipsoidal particle in a shear flow. J. Fluid Mech. 120 27–47.
- Khodadad JK, Weinstein RS. The band 3-rich membrane of llama erythrocytes: studies on cell shape and the organization of membrane proteins.. J Membr Biol 1983;72(3):161-71.
- Khodadad JK, Weinstein RS. Band 3 protein of the red cell membrane of the llama: crosslinking and cleavage of the cytoplasmic domain.. Biochem Biophys Res Commun 1985 Jul 16;130(1):493-9.
- Kumar A, Henriquez Rivera R G, Graham M. Flow induced segregation in confined multicomponent suspensions: effects of particle size and rigidity. J. Fluid Mech. 738 423–462.
- Lee BK, Alexy T, Wenby RB, Meiselman HJ. Red blood cell aggregation quantitated via Myrenne aggregometer and yield shear stress.. Biorheology 2007;44(1):29-35.
- Lim G, Wortis M, Mukhopadhyay R. Red blood cell shapes and shape transformations: newtonian mechanism of a composite membrane. .
- Lorkin PA. Fetal and embryonic haemoglobins.. J Med Genet 1973 Mar;10(1):50-64.
- Lux SE 4th. Anatomy of the red cell membrane skeleton: unanswered questions.. Blood 2016 Jan 14;127(2):187-99.
- Manno S, Takakuwa Y, Mohandas N. Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation.. J Biol Chem 2005 Mar 4;280(9):7581-7.
- Maretzki D, Reimann B, Rapoport SM. A reappraisal of the binding of cytosolic enzymes to erythrocyte membranes.. Trends Biochem Sci 1989 Mar;14(3):93-6.
- Matei H, Frentescu L, Benga G. Comparative studies of the protein composition of red blood cell membranes from eight mammalian species.. J Cell Mol Med 2000 Oct-Dec;4(4):270-276.
- McPherson RA, Sawyer WH, Tilley L. Band 3 mobility in camelid elliptocytes: implications for erythrocyte shape.. Biochemistry 1993 Jul 6;32(26):6696-702.
- Mezger T G. Das Rheologie Handbuch, 3rd Edn. Hannover: Vincentz Network.
- Moore D M. Haematology of camelid species: ilamas and camels. in Schalm’s Veterinary Haematology, 5th Edn, 1184–1190.
- Nakao M. New insights into regulation of erythrocyte shape.. Curr Opin Hematol 2002 Mar;9(2):127-32.
- Omorphos SA, Hawkey CM, Rice-Evans C. The elliptocyte: a study of the relationship between cell shape and membrane structure using the camelid erythrocyte as a model.. Comp Biochem Physiol B 1989;94(4):789-95.
- Persson S G B. The significance of hematological data in the evaluation of soundness and fitness in the horse. in Equine Exercise Physiology, 324–338.
- Peters S. Vollblutviskosität Beim Pferd in Abhängigkeit von Hämatokrit und Temperatur. Vienna: Veterinary University of Vienna; M.Sc thesis.
- Plasenzotti R, Stoiber B, Posch M, Windberger U. Red blood cell deformability and aggregation behaviour in different animal species.. Clin Hemorheol Microcirc 2004;31(2):105-11.
- Plasenzotti R, Windberger U, Ulberth F, Osterode W, Losert U. Influence of fatty acid composition in mammalian erythrocytes on cellular aggregation.. Clin Hemorheol Microcirc 2007;37(3):237-43.
- R Core Team. A Language and Environment for Statistical Computing. Vienna: Foundation for Statistical Computing.
- Ralston GB. Proteins of the camel erythrocyte membrane.. Biochim Biophys Acta 1975 Aug 5;401(1):83-94.
- Reinhart WH, Chien S. Red cell rheology in stomatocyte-echinocyte transformation: roles of cell geometry and cell shape.. Blood 1986 Apr;67(4):1110-8.
- Rogalski AA, Steck TL, Waseem A. Association of glyceraldehyde-3-phosphate dehydrogenase with the plasma membrane of the intact human red blood cell.. J Biol Chem 1989 Apr 15;264(11):6438-46.
- Rose RJ, Evans DL, Henckel P, Knight PK, Cluer D, Saltin B. Metabolic responses to prolonged exercise in the racing camel.. Acta Physiol Scand Suppl 1994;617:49-60.
- Russel W B, Saville D A, Schowalter W R. Colloidal Dispersions. New York, NY: Cambridge University Press.
- Omodeo Salè F, Vanzulli E, Caielli S, Taramelli D. Regulation of human erythrocyte glyceraldehyde-3-phosphate dehydrogenase by ferriprotoporphyrin IX.. FEBS Lett 2005 Sep 12;579(22):5095-9.
- Satchwell TJ, Shoemark DK, Sessions RB, Toye AM. Protein 4.2: a complex linker.. Blood Cells Mol Dis 2009 May-Jun;42(3):201-10.
- SCHMIDT-NIELSEN K. The physiology of the camel.. Sci Am 1959 Dec;201:140-51.
- Schuler B, Arras M, Keller S, Rettich A, Lundby C, Vogel J, Gassmann M. Optimal hematocrit for maximal exercise performance in acute and chronic erythropoietin-treated mice.. Proc Natl Acad Sci U S A 2010 Jan 5;107(1):419-23.
- Sens P, Gov N. Force balance and membrane shedding at the red-blood-cell surface.. Phys Rev Lett 2007 Jan 5;98(1):018102.
- Sirover MA. New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase.. Biochim Biophys Acta 1999 Jul 13;1432(2):159-84.
- Skotheim JM, Secomb TW. Red blood cells and other nonspherical capsules in shear flow: oscillatory dynamics and the tank-treading-to-tumbling transition.. Phys Rev Lett 2007 Feb 16;98(7):078301.
- Smith JE, Mohandas N, Shohet SB. Variability in erythrocyte deformability among various mammals.. Am J Physiol 1979 May;236(5):H725-30.
- Stoiber B, Zach C, Izay B, Windberger U. Whole blood, plasma viscosity, and erythrocyte aggregation as a determining factor of competitiveness in standard bred trotters.. Clin Hemorheol Microcirc 2005;32(1):31-41.
- Strutz T. Data Fitting and Uncertainty: A Practical Introduction to Weighted Least-Squares and Beyond, 2nd Edn. Wiesbaden: Springer.
- Tinson A. The Camel: The Animal of the 21th Century. Bikaner: Camel Publishing House.
- Tomaiuolo G, Lanotte L, Ghigliotti G, Misbah C, Guido S. Red blood cell clustering in poiseuille microcapillary flow. Phys. Fluids 24:051903.
- Tran-Son-Tay R, Sutera SP, Rao PR. Determination of red blood cell membrane viscosity from rheoscopic observations of tank-treading motion.. Biophys J 1984 Jul;46(1):65-72.
- Tsai IH, Murthy SN, Steck TL. Effect of red cell membrane binding on the catalytic activity of glyceraldehyde-3-phosphate dehydrogenase.. J Biol Chem 1982 Feb 10;257(3):1438-42.
- Ugwu C P, Abarshi M M, Mada S B, Sanusi B, Nzelibe H C. Camel and horse milk casein hydrolysates exhibit angiotensin converting enzyme inhibitory and antioxidative effects in vitro and in silico. Int. J. Peptide Res. Therapeutics 2019 1–10.
- Usami S, Magazinovic V, Chien S, Gregersen MI. Viscosity of turkey blood: rheology of nucleated erythrocytes.. Microvasc Res 1970 Oct;2(4):489-99.
- VERWEY EJ. Theory of the stability of lyophobic colloids.. J Phys Colloid Chem 1947 May;51(3):631-6.
- Wagner N J, Brady J F. Shear thickening in colloidal dispersions. Phys. Today 62 27–32.
- Warda M, Zeisig R. Phospholipid- and fatty acid-composition in the erythrocyte membrane of the one-humped camel [Camelus dromedarius] and its influence on vesicle properties prepared from these lipids.. Dtsch Tierarztl Wochenschr 2000 Sep;107(9):368-73.
- Warren JR, Harris AS, Wallas CH. Transformation of human erythrocyte shape by endotoxic lipopolysaccharide.. Infect Immun 1983 Jan;39(1):431-4.
- Waugh R E. Red cell deformability in different vertebrate animals. Clin. Hemorheol. 12 649–656.
- Weiss D J, Geor R J. Clinical and rheological implications of echinocytosis in the horse: a review. Comp. Haematol. Int. 3 185–189.
- Weiss DJ, Geor RJ, Smith CM 2nd. Effects of echinocytosis on hemorrheologic values and exercise performance in horses.. Am J Vet Res 1994 Feb;55(2):204-10.
- Weiss DJ, Moritz A. Equine immune-mediated hemolytic anemia associated with Clostridium perfringens infection.. Vet Clin Pathol 2003;32(1):22-6.
- Wernery U, Fowler M E, Wernery R. Color Atlas of Camelid Hematology. Berlin: Blackwell, 78.
- Williams T, Kelley C, Crawford D. Gnuplot 5.2: An Interactive Plotting Program. Suwanee, GA: 12th Media Services.
- Windberger U. Animal blood suspensions. in Suspension Dynamics of Blood Cells in Microflows.
- Windberger U, Bartholovitsch A, Plasenzotti R, Korak KJ, Heinze G. Whole blood viscosity, plasma viscosity and erythrocyte aggregation in nine mammalian species: reference values and comparison of data.. Exp Physiol 2003 May;88(3):431-40.
- Windberger U, Stoiber B, Poeschl C, van den Hoven R. A comparative approach to measure elasticity of whole blood by small amplitude oscillation. Rheol Open Access 1:103.
- Wirther J L, Noguchi H, Gompper G. Ordering and arrangement of deformed red blood cells in flow through microcapillaries. New. J. Phys. 14:085026.
- Yamaguchi K, Jürgens KD, Bartels H, Piiper J. Oxygen transfer properties and dimensions of red blood cells in high-altitude camelids, dromedary camel and goat.. J Comp Physiol B 1987;157(1):1-9.
- Zhang J. Effect of suspending viscosity on red blood cell dynamics and blood flows in microvessels.. Microcirculation 2011 Oct;18(7):562-73.
- Zhang Z, Chien W, Henry E, Fedosov D A, Gompper G. Sharp-edged geometric obstacles in microfluidics promote deformability-based sorting of cells. Phys. Rev. Fluids 4:024201.
Citations
This article has been cited 2 times.- Pesen T, Haydaroglu M, Capar S, Parlatan U, Unlu MB. Comparison of the human's and camel's red blood cell deformability by optical tweezers and Raman spectroscopy.. Biochem Biophys Rep 2023 Sep;35:101490.
- Baier D, Müller T, Mohr T, Windberger U. Red Blood Cell Stiffness and Adhesion Are Species-Specific Properties Strongly Affected by Temperature and Medium Changes in Single Cell Force Spectroscopy.. Molecules 2021 May 8;26(9).
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