William W. Muir
Dez Hughes2†
Deborah C. Silverstein- 1College of Veterinary Medicine, Lincoln Memorial University, Harrogate, TN, United States
- 2Melbourne Veterinary School, Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Melbourne, VIC, Australia
- 3Department of Clinical Sciences and Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA, United States
Editorial on the Research Topic
Fluid Therapy in Animals: Physiologic Principles and Contemporary Fluid Resuscitation Considerations
Introduction
What an oversight! Fluids are drugs (1), so why has one of the most administered, and arguably beneficial, therapies employed in veterinary medicine been so inadequately investigated? Intravenous fluids (i.e., drug) can produce positive or negative effects dependent upon their dose and the circumstances (i.e., context) that exist when they are administered (2, 3). Improved understanding of the physiologic principles that determine the effects and consequences of fluid therapy in healthy and diseased animals is essential to good clinical practice (4–86). Notably, most of the “evidence” investigating fluid therapy in animals has been obtained from studies that are not randomized, properly controlled, blinded, adequately powered, or fail to identify predefined primary or secondary outcomes (73, 75, 87, 88). As a result, much of the medical literature provides, “little reliable information on the effectiveness of fluid resuscitation” in diverse clinical scenarios (2, 3, 89–93). Future studies must address these limitations since “fluid therapy might be more difficult than you think” (94), “nothing is more dangerous than conscientious foolishness” (95) and “solely the dose determines that a thing is not a poison” (96). For example, the pharmacokinetics of fluids administered to cats, dogs, horses, or cattle are largely unknown and generally not considered when designing fluid therapy trials although it has been addressed in the human medical literature for more than 20 years (31, 97–100).
This issue of Frontiers in Veterinary Science provides: (1) A review of the terms used to define or describe fluid therapy (Chow); (2) An update on body fluid compartments and the physiological concepts that guide fluid therapy (Stewart; Woodcock and Michel; Smart and Hughes; Cooper and Silverstein); (3) A discussion of fluid kinetics and its relevance to fluid administration in cats (Yiew, Bateman, Hahn, Bersenas, Muir; Yiew, Bateman, Hahn, Bersenas); (4) Contemporary recommendations for the administration of IV fluid regimens in small and large animals (Rudloff and Hopper; Crabtree and Epstein; Adamik and Yozova); (5) The effects of IV fluids on the coagulation system (Boyd et al.); (6) A discussion of fluid administration in animals with naturally occurring disorders and diseases (e.g., food deprivation, dehydration, sepsis, renal, pulmonary, trauma, hemorrhage, traumatic brain injury; Freeman; Dias et al.; Montealegre and Lyons; Constable et al.; Hall and Drobatz; Pigot and Rudloff; Langston and Gordon; Adamantos) including refractory hypotension (Valverde) and cardiopulmonary resuscitation (Fletcher and Boller); (7) The consequences of fluid overload (Hansen); (8) A description of dynamic fluid therapy monitoring techniques (Boysen and Gommeren); (9) An introduction to fluids of the future (Edwards and Hoareau); and (10) Alternative methods for fluid delivery (Gholami et al.). The information and citations contained within this collection serve as a rich resource for the design of future studies investigating the safety and efficacy of intravenous fluid therapy in animals.
Body Fluid Compartments
Water (i.e., total body water: TBW) is responsible for ~60–70% of body weight (BW) and is the primary component of all body fluids (101). The two main body fluid compartments are the intracellular fluid (ICF) and extracellular fluid (ECF). Approximately two-thirds (≈40%) of TBW is intracellular fluid (ICF) and one-third (≈20%) extracellular fluid (ECF). The ECF is comprised of four sub-compartments, the intravascular fluid volume (i.e., plasma volume: PV; 4–5% BW), the fluid that surrounds cells (i.e., interstitial fluid volume: IFV; ≈15–18% BW), lymph, and fluids contained within epithelial lined spaces (transcellular fluids) [Stewart; (101–104)]. Severe obesity can increase the relative percentage of the ECF by up to 50% of TBW (≈ 30% BW) (105). The intravascular volume (i.e., blood volume: BV) is comprised of the red cell volume (RBCV; 6–8% BW) and plasma volume (PV) (106, 107). If the packed red blood cell volume (PCV) is known BV can be determined (i.e., BV = PV × 100/100-PCV) (106). Transcellular fluids are infrequently considered when determining water and solute requirements in simple stomached animals but become important in horses and ruminants (108). Determination of the body's fluid compartments is technically challenging, time consuming, and often inaccurate (109–111). Substances used for this purpose (i.e., “dilutional tracer technique”) must be non-toxic, easily detectable and sustain a steady state concentration within the compartment (112–114).
Contemporary evidence suggests that the PV is comprised of circulating and non-circulating (15–25% of PV) components, the latter being located within an endothelial surface or glycocalyx layer (GLX) and the channels between vascular epithelial cells (115, 116). The GLX interacts freely with plasma proteins and acts as an surface layer “gatekeeper” for larger molecules selectively reducing plasma solute distribution volume dependent upon their molecular weight (MW), shape (i.e., effective molecular radius), electrical charge, and concentration (11–14, 117). Crystalloids have a shorter intravascular retention time than colloids (100, 118–121).
Blood Distribution
Blood volume is distributed between the pulmonary (18–20%) and systemic (78–80%) circulations dependent upon their (e.g., brain, heart, lung, and gut) oxygen requirements (VO2). Veins are ~30 times more compliant than arteries, contain up to five times more adrenergic receptors than arteries and normally serve as blood reservoirs (122). Some investigators have described the blood volume contained within the systemic veins as either unstressed or stressed (123, 124). The unstressed volume (Vu; ≈70% BV) is equivalent to the blood volume required to fill the veins without increasing the transmural pressure above zero mmHg and the stressed volume (Vs; ≈30% BV) as the volume of blood required to increase the transmural pressure to values above zero (123). Under normal circumstances Vu is believed to serve as a reserve volume that can be mobilized by increasing sympathetic activity (i.e., alpha 1 receptors) thereby increasing vs. (i.e., “effective” BV) (125, 126). The mean circulatory filling pressure (MCFP) is defined as the mean vascular pressure that exists in the systemic circulation after the heart is stopped and is argued to be determinant of venous return and cardiac output (127, 128). A growing number of vascular physiologists however consider this interpretation to be abstract and erroneous opting to believe that cardiac contraction is the independent variable that drives blood flow and determines cardiac output (129–136).
Water Balance
Water balance (i.e., water intake and output) is governed by a variety of neural and neuroendocrine high-gain homeostatic feedback mechanisms that include, osmoreceptors, osmotically stimulated thirst receptors, hormones [e.g., renin-angiotensin-aldosterone system (RAAS), angiotensin-converting enzyme-2 (ACE2)/angiotensin 1–7 (Ang 1–7), vasopressin (antidiuretic hormone: ADH), erythropoietin (EPO), atrial natriuretic peptide (ANP)] and membrane water channels (i.e., aquaporins), especially those located in the renal tubules (137–144). The kidney is responsible for regulating fluid, electrolyte balance and blood volume (145–147). The kidney also produces and secrets erythropoietin (e.g., low Hb, PaO2, flow) signaling bone marrow to produce more red blood cells. Activated atrial stretch receptors secrete ANP producing vasodilation and increases in glomerular filtration, salt and water excretion, and vascular permeability, thereby regulating PV and lowering arterial blood pressure (ABP) (141, 148). Therefore, the kidney is regarded as a key determinant of both PV and BV. Negatively charged glycosaminoglycans (GAGs) located in the interstitial spaces and lymphatics of the skin also function as non-renal regulators of sodium ion concentration and ECF volume (7, 8) serving as indirect controllers of arterial blood pressure (ABP) by shifting fluid from the interstitial to the intravascular space (7, 8, 149).
Blood Flow and Tissue Perfusion
The heart and vasculature deliver blood to and from the systemic and pulmonary circulations and, in conjunction with interstitial compliance and the lymphatic system, are responsible for ensuring the continuous circulation of fluid throughout the body (5, 5, 150–156). Three categories of capillaries are involved in the exchange of fluid, gases (O2, CO2), and solutes (e.g., albumin) (155, 157). Non-fenestrated or continuous capillaries nourish the tissues of the nervous system, muscle, connective tissue, skin, lung, and fat. Fenestrated (i.e., contain “pores”) capillaries perfuse the kidneys, intestinal mucosa, synovial linings, exocrine glands and sinusoidal or discontinuous capillaries with large intercellular breaks (i.e., pores) filter blood in the liver, spleen, and bone marrow (11). All three are coated to a greater or lesser extent by the semi-permeable negatively charged GLX [(11–13); [Yiew, Bateman, Hahn, Bersenas; Rudloff and Hopper; Crabtree and Epstein; Adamik and Yozova; (155, 158)]. Plasma filtration among the different types of capillaries is determined by hydrostatic (mmHg) and osmotic (mOsm/L) pressures, the number and size or their fenestrations [i.e., “pores”]), capillary surface area, the thickness of the GLX, the pre- to postcapillary vascular tone (i.e., resistance ratio), and tissue compliance (3, 159–162). Capillaries in the renal glomeruli are fenestrated (pore: 30–60 nm) but have a smaller effective pore size (pore: ≤ 15 nm) due to the influence of the GLX on the filtration of larger (>40–50 kDa) molecules (163, 164). Non-fenestrated capillaries (e.g., central nervous system blood brain barrier; ≤ 1–2 nm) with numerous endothelial transport vesicles enable transcytosis (i.e., transcellular transport of macromolecules). They are less permeable to fluid and electrolyte exchange than fenestrated capillaries, although water and small solutes pass through endothelial intercellular clefts in accordance with hydrostatic pressure differences (157). Non-fenestrated “continuous” capillaries (e.g., skin, lungs, and the blood-brain barrier) have a comparatively small effective pore size (pore: 3–5 nm) that inhibits the trans-vascular flux of fluid and most solutes (160, 163–165).
The GLX constitutes ~2% of the PV and functions as two layers: a less permeable, dense branch-like inner layer composed of heparin sulfate and glycoproteins and a more permeable porous outer later composed of plasma proteins and glycosaminoglycans (13, 104, 166). The GLX limits albumin (i.e., large molecule) and RBC access, leukocyte contact with the inner layer and endothelial surface (13, 104, 166), participates in cell signaling (i.e., nitric oxide-induced vasorelaxation), provides anti-coagulant effects and protects endothelial cells from oxidative stress (107). Small molecules, such as water, gases, small lipids, and lipid-soluble molecules diffuse freely through the GLX through endothelial intercellular clefts or by facilitated diffusion (158). Larger molecules (i.e., colloids) negligibly penetrate the GLX and distribute in a smaller intravascular volume than crystalloids which readily distribute throughout the entire intravascular space. Recent studies suggest that crystalloid-to-colloid ratios should range from 0.7 to 1.4:1 in contrast to older ratios (i.e., 1:3) (167–175) and that crystalloid-to-blood ratios > 1:1 produce perivascular edema, pulmonary parenchymal stiffness (176), impaired coagulation [Boyd et al.; (177, 178)], increased blood loss (44), and increased vasopressor requirements (43). Disagreements favoring colloids over crystalloids rest more on their delayed diffusion than on their safety [(44, 50–53); Boyd et al.; (179)], risk-benefit ratio (Adamik and Yozova) or cost.
Transvascular Fluid Flux
Traditional Theory
The dynamics of fluid flux (Jv) across capillary walls is historically attributed to Earnest Starling's observations of fluid absorption from connective tissue spaces (Starling 1896) (180). He concluded that capillary hydrostatic pressure was responsible for transudation of a small amount of fluid into the tissues (“frictional resistance of the capillary wall”), thereby forming lymph, and that the colloid osmotic pressure produced by plasma proteins was responsible for fluid absorption. He also postulated that the forces moving fluid in and out of the capillary were almost balanced. Subsequent experiments resulted in mathematical descriptions of Starling's hypothesis and suggested equations wherein Jv (i.e., transvascular fluid flux) is a balance of intravascular capillary (c) intravascular and interstitial (i) hydraulic (i.e., hydrostatic pressure: P) and oncotic [π: colloid osmotic pressure (COP)] forces (Kedem–Katchalski equations) (181). Capillary hydrostatic pressure (Pc) is a function of the hydrostatic P from the inflow (arterial: a) to the outflow (venous: v) end of the capillary and are dependent upon the pre- and post-capillary resistances (R), assuming blood flow remains constant (182–186). A decrease in Ra (e.g., arteriolar vasodilation) or an increase in Rv (venoconstriction) decreases Ra/Rv and increases both Pc and Jv (3). Under normal circumstances Pc is more sensitive to changes in Pv than Pa but during intense arterial vasoconstriction, Pc decreases rapidly (increased Ra/Rv) (3, 185). Plasma proteins are responsible for generating πc and COP is the hydrostatic pressure required to prevent fluid movement into the plasma or, alternatively, the pressure that pulls fluid across the capillary wall into the plasma. Capillary Pc (i.e., hydraulic push) is therefore opposed by capillary πc [i.e., osmotic suction: (Pc - πc)] and Pi is opposed by πi (Pi - πi). The Starling hypothesis asserts that fluid is filtered at the arterial end of the capillary because Pc predominates over all other forces, and that fluid is reabsorbed at the venous end of the capillary because πc (osmotic suction) predominates. Interstitial forces (Pi, πi) act as modulators of the rate of fluid flux and therefore the volume of Jv (14, 185). Later studies modified Starling's hypothesis to account for transvascular fluid flux rates per unit pressure (i.e., hydraulic conductance: Lp) and the macromolecular sieving properties of the microvascular barrier (Staverman's reflection coefficient: σ) [(12–14); Woodcock and Michel; (173, 187)]. Both Lp and σ vary among different types of capillaries since Lp is dependent upon the number of “pores” and σ is dependent on effective pore diameter. The σ for most plasma solutes ranges from 0 to 1 (i.e., 0 = totally permeable; 1 = totally impermeable) (187). The capillary wall osmotic and σ for water, anions, cations, and smaller soluble substances like glucose is nearly 0 (freely permeable) (160). Larger plasma solutes (>30–40 kDa), like albumin (66–69 kDa; diameter ~3.5 nm), which accounts for 80% of total plasma protein and commercial semisynthetic colloid solutions (i.e., gelatins, dextran, and hydroxyethyl starches; COP range 24–60 mm Hg) exhibit σ's ranging from 0.7 to 1.0 and are almost impermeant to most the microvascular barrier except the sinusoids of the liver. The incorporation of Lp and σ into Starlings hypothesis is the basis for what is proclaimed as the “Starling equation” that is still published in most texts [Jv = Lp [(Pc – Pi) – σ (πc – πi)]], although Starling had little to do with its derivation since the earliest form of the equation did not appear until 1927 (182).
Contemporary Theory
Recent investigations have led to a revision of the Starling hypothesis (165) and the Starling equation based upon GLX COP (πg): Jv = Lp [(Pc – Pi) – σ (πc – πg)] [(11); Woodcock and Michel; (188–193)]. It is now realized that the interstitial COP does not directly determine fluid movement across the microvascular wall, and that the effect of πc on Jv is far less than originally predicted (11, 189–195). The sieving properties of the glycocalyx modify Starling's forces by imposing an obstacle to Jv. The π difference across non-fenestrated capillaries is influenced by the πg and πi is far less important in determining Jv than originally proposed. Notably, πg is negligible compared to πc such that the osmotic pressure gradient across the glycocalyx is close to πc rather than the difference between πc and πi. Fluid that is filtered through the glycocalyx flows rapidly through narrow inter-endothelial cell breaks, thereby limiting interstitial protein back diffusion into the sub-glycocalyx space. The “Revised” Starling equation [(11); Woodcock and Michel; (189)] has proven to be more consistent with experimental and clinical observations and suggests that (1) Jv is far less than originally predicted; (2) Fluid is not normally reabsorbed from the venous end of the capillary during normal physiologic conditions (steady state no-reabsorption rule); (3) Tissue lymph drainage is the primary route for return of interstitial fluid to the circulation; (4) Interstitial fluid is reabsorbed from the interstitium when Pc decreases until a new steady state is established (14); and (5) Crystalloid is almost as effective as a colloid (Col) administration for treating hypovolemia from blood loss (11, 173–176). These revisions highlight the importance of GLX composition and integrity and the number of inter-endothelial cellular “breaks” (i.e., glycocalyx-junction-break model) in determining the effectiveness of fluid resuscitation (195). They do not negate the “importance of transcapillary refill” as suggested by some (196), but do have important implications regarding fluid selection, rate, and volume for improving fluid efficiency and effectiveness in diseased animals [Woodcock and Michel; (189, 194, 197)].
Volume Kinetics
Volume kinetics (VK) determines the volume into which an administered fluid is distributed (i.e., volume of distribution: Vd), the volume of plasma that is completely cleared of the administered fluid per unit time (i.e., clearance: Cl) and the time it takes for the total amount of administered fluid to be reduced by one-half of its original volume (i.e., half-life: t1/2) (31). Intravenous fluids are initially distributed into a central compartment (Vc) followed by diffusion into a peripheral compartment (Vt) [(31); Yiew, Bateman, Hahn, Bersenas, Muir; (179, 198–201)]. The distribution half-time for most crystalloids is relatively short (<8–10 min) implying that distribution is complete within ~30–50 min (4–5 half-lives), a range that closely coincides with the measured half-lives reported for acetated (56 min) and lactated (50 min) Ringer's solutions in humans (155). A low Cld from Vc increases the infused fluid's potency (i.e., the volume required to expand the plasma volume by 20% in 30 min) but also increases hemodilution. The Cld for colloidal solutions [i.e., hydroxyethyl starches (HES)] is much lower than crystalloids, suggesting delayed departure from Vc and prolongation of their volume expanding effects.
Rapid fluid administration rates (>40–60 ml/kg/hr) and large fluid volumes (>60–80 ml/kg) produce hemodilution, interstitial fluid accumulation (i.e., edema), and serious rebleeding in animals with uncontrolled hemorrhage (15, 78, 83, 202, 203). Most anesthetic drugs, particularly inhalant anesthetics (e.g., propofol, isoflurane), depress cardiorespiratory function, blunt homeostatic reflexes, promote vasoplegia, [Valverde; (204–206)] decrease tolerance to acute anemia [i.e., increase the critical Hb concentration: (Hbcrit)] (207, 208), promote interstitial fluid accumulation (209) and perioperative fluid retention (209–212), decrease urine output (212, 213), and depress the response to fluid administration (204, 214). In addition, vasoactive drugs are known to alter fluid volume kinetics (215–219). Stimulation of alpha1- adrenergic receptors (e.g., norepinephrine; phenylephrine) increases Vd, Cld, the accumulation of fluid in Vt, and Clr while stimulation of beta-1 adrenergic receptors (e.g., isoproterenol) increase Vc and decrease Vd, Cld, and Clr (69, 216, 217, 220). Notably, fluid accumulation in Vt is more significantly influenced by the rate of infusion (i.e., ml/kg/min) than by the infused fluid volume; higher infusion rates produce greater degrees of interstitial fluid accumulation, hemodilution, coagulation abnormalities, and organ dysfunction (79, 199, 203, 221, 222).
New Horizons
New fluids and goal directed fluid therapies (GDFT) continue to be developed for the treatment of specific naturally occurring diseases with the goals of improving tissue oxygenation and perfusion [(9); Edwards and Hoareau; (197, 223–228)], and reducing adverse events and mortality (229, 230). Damage control resuscitation (DCR) strategies limit the amount of crystalloids administered and employ balanced blood product resuscitation ratios [PRBC's-plasma-platelets ratio of 1:1:1; Hall and Drobatz; Boysen and Gommeren; (230–235)]. Isotonic and hypertonic crystalloid solutions continue to be investigated in order to rapidly restore hemodynamics, reduce the amount of fluid administered in order minimize hemodilution, and tissue edema, and lessen the development of disseminated intravascular coagulation (58–62, 236, 237). Novel therapies that mimic natural hemostatic mechanisms (68) or reduce vascular leakage (238–240) are being developed and solutions that increase tissue oxygenation (e.g., hemoglobin) and restore microcirculatory blood flow continue to evolve (241–243). Future fluids should protect or repair the endothelium (224, 228, 238, 244, 245). Methods for determining their success will be dependent upon the development of validated dynamic non or minimally invasive hemodynamic monitoring methodologies [(42); Cooper and Silverstein; Boysen and Gommeren; (20, 38–41, 235, 246–254)] in addition assessment of thromboelastographic variables (249), implementation of deep-learning algorithms (254) and development of bio-responsive drug delivery systems [Gholami et al.; (255–260)]. It is hoped that the information contained within this compendium will inspire readers to employ fluid therapy practices that improve patient outcome.
Author Contributions
All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Acknowledgments
We acknowledge Lincoln Memorial University College of Veterinary Medicine, Dechra Veterinary Products, and Nova Biomedical for support of this project.
References
1. Raghunathan K, Shaw AD, Bagshaw SM. Fluids are drugs: type, dose and toxicity. Curr Opin Crit Care. (2013) 19:290–8. doi: 10.1097/MCC.0b013e3283632d77
2. James MFM. Context-sensitive fluid administration: what, when and how much. South Afr J Anaesth Analges. (2015) 21:38–9.
3. Tatara T. Context-sensitive fluid therapy in critical illness. J Intensive Care. (2016) 4:20. doi: 10.1186/s40560-016-0150-7
4. Uemura K, Sugimachi M, Kawada T, Kamiya A, Jin Y, Kashihara K, et al. A novel framework of circulatory equilibrium. Am J Physiol Heart Circ Physiol. (2004) 286:H2376–85. doi: 10.1152/ajpheart.00654.2003
5. Breslin JW, Yang Y, Scallan JP, Sweat RS, Adderley SP, Murfee WL. Lymphatic vessel network structure and physiology. Compr Physiol. (2018) 9:207–99. doi: 10.1002/cphy.c180015
6. Jessen NA, Munk AS, Lundgaard I, Nedergaard M. The glymphatic system: a beginner's guide. Neurochem Res. (2015) 40:2583–99. doi: 10.1007/s11064-015-1581-6
7. Wiig H, Luft FC, Titze JM. The interstitium conducts extrarenal storage of sodium and represents a third compartment essential for extracellular volume and blood pressure homeostasis. Acta Physiol. (2018) 222:13006. doi: 10.1111/apha.13006
8. Minegishi S, Luft FC, Titze J, Kitada K. Sodium handling and interaction in numerous organs. Am J Hypertens. (2020) 33:687–96. doi: 10.1093/ajh/hpaa049
9. Ince C, Ertmer C. Hemodynamic coherence: its meaning in perioperative and intensive care medicine. Best Pract Res Clin Anaesthesiol. (2016) 30:395–7. doi: 10.1016/j.bpa.2016.11.004
10. Guven G, Hilty MP, Ince C. Microcirculation: physiology, pathophysiology, and clinical application. Blood Purif. (2020) 49:143–50. doi: 10.1159/000503775
11. Woodcock TE, Woodcock TM. Revised Starling equation and the glycocalyx model of transvascular fluid exchange: an improved paradigm for prescribing intravenous fluid therapy. Br J Anaesth. (2012) 108:384–94. doi: 10.1093/bja/aer515
12. Jiang XZ, Ventikos Y, Luo KH. Microvascular ion transport through endothelial glycocalyx layer: new mechanism and improved Starling principle. Am J Physiol Heart Circ Physiol. (2019) 317:H104–13. doi: 10.1152/ajpheart.00794.2018
13. Gaudette S, Hughes D, Boller M. The endothelial glycocalyx: structure and function in health and critical illness. J Vet Emerg Crit Care. (2020) 30:117–34. doi: 10.1111/vec.12925
14. Michel CC, Woodcock TE, Curry FE. Understanding and extending the Starling Principle. Acta Anaesthesiol Scand. (2020) 64:1032–7. doi: 10.1111/aas.13603
15. Hahn RG. Fluid therapy in uncontrolled hemorrhage–what experimental models have taught us. Acta Anaesthesiol Scand. (2013) 57:16–28. doi: 10.1111/j.1399-6576.2012.02763.x
16. Perner A, Junttila E, Haney M, Hreinsson K, Kvåle R, Vandvik PO, et al. Scandinavian Society of Anaesthesiology and Intensive Care Medicine: scandinavian clinical practice guideline on choice of fluid in resuscitation of critically ill patients with acute circulatory failure. Acta Anaesthesiol Scand. (2015) 59:274–85. doi: 10.1111/aas.12429
17. Marik P, Bellomo R. A rational approach to fluid therapy in sepsis. Br J Anaesth. (2016) 116:339–49. doi: 10.1093/bja/aev349
18. Voldby AW, Brandstrup B. Fluid therapy in the perioperative setting—a clinical review. J Intensive Care. (2016) 4:27. doi: 10.1186/s40560-016-0154-3
19. Wise R, Faurie M, Malbrain MLNG, Hodgson E. Strategies for intravenous fluid resuscitation in trauma patients. World J Surg. (2017) 41:1170–83. doi: 10.1007/s00268-016-3865-7
20. Joosten A, Raj Lawrence S, Colesnicenco A, Coeckelenbergh S, Vincent JL, Van der Linden P, et al. Personalized versus protocolized fluid management using noninvasive hemodynamic monitoring (clearsight system) in patients undergoing moderate-risk abdominal surgery. Anesth Analg. (2019) 129:e8–e12. doi: 10.1213/ANE.0000000000003553
21. Ramesh GH, Uma JC, Farhath S. Fluid resuscitation in trauma: what are the best strategies and fluids? Int J Emerg Med. (2019) 12:38. doi: 10.1186/s12245-019-0253-8
22. Marik PE, Weinmann M. Optimizing fluid therapy in shock. Curr Opin Crit Care. (2019) 25:246–51. doi: 10.1097/MCC.0000000000000604
23. Zimmerman RA, Tsai AG, Intaglietta M, Tartakovsky DM. A mechanistic analysis of possible blood transfusion failure to increase circulatory oxygen delivery in anemic patients. Ann Biomed Eng. (2019) 47:1094–105. doi: 10.1007/s10439-019-02200-9
24. Keijzers G, Macdonald SP, Udy AA, Arendts G, Bailey M, Bellomo R, et al. ARISE FLUIDS Observational Study Group. The Australasian Resuscitation In Sepsis Evaluation: Fluids or vasopressors in emergency department sepsis (ARISE FLUIDS), a multi-centre observational study describing current practice in Australia and New Zealand. Emerg Med Australas. (2019) 32:90–6. doi: 10.1111/1742-6723.13223
25. Malbrain MNG, Van Regenmortel N, Saugel B, Tavernier B, Van Gaal PJ, Joannes-Boyau O, et al. Principles of fluid management and stewardship in septic shock: it is time to consider the four D's and the four phases of fluid therapy. Ann Intensive Care. (2018) 8:66. doi: 10.1186/s13613-018-0402-x
26. Spiegel R, Gordon D, Marik PE. The origins of the Lacto-Bolo reflex: the mythology of lactate in sepsis. J Thorac Dis. (2020) 12:S48–53. doi: 10.21037/jtd.2019.11.48
27. Lira A, Pinsky MR. Choices in fluid type and volume during resuscitation: impact on patient outcomes. Ann Intensive Care. (2014) 4:38. doi: 10.1186/s13613-014-0038-4
29. Bennett VA, Cecconi M. Perioperative fluid management: from physiology to improving clinical outcomes. Indian J Anaesth. (2017) 61:614–21. doi: 10.4103/ija.IJA_456_17
30. Lewis SR, Pritchard MW, Evans DJ, Butler AR, Alderson P, Smith AF, et al. Colloids versus crystalloids for fluid resuscitation in critically ill people. Cochrane Database Syst Rev. (2018) 8:CD000567. doi: 10.1002/14651858.CD000567.pub7
31. Hahn RG. Understanding volume kinetics. Acta Anaesthesiol Scand. (2020) 64:570–8. doi: 10.1111/aas.13533
32. Bundgaard-Nielsen M, Holte K, Secher NH, Kehlet H. Monitoring of peri-operative fluid administration by individualized goal-directed therapy. Acta Anaesthesiol Scand. (2007) 51:331–40. doi: 10.1111/j.1399-6576.2006.01221.x
33. Marik PE. Fluid responsiveness and the six guiding principles of fluid resuscitation. Crit Care Med. (2016) 44:1920–2. doi: 10.1097/CCM.0000000000001483
34. Monnet X, Marik PE, Teboul JL. Prediction of fluid responsiveness: an update. Ann Intensive Care. (2016) 6:111. doi: 10.1186/s13613-016-0216-7
35. Martin ND, Codner P, Greene W, Brasel K, Michetti C, AAST Critical Care Committee. Contemporary hemodynamic monitoring, fluid responsiveness, volume optimization, and endpoints of resuscitation: an AAST critical care committee clinical consensus. Trauma Surg Acute Care Open. (2020) 5:e000411. doi: 10.1136/tsaco-2019-000411
36. Shi R, Monnet X, Teboul JL. Parameters of fluid responsiveness. Curr Opin Crit Care. (2020) 22:723. doi: 10.1097/MCC.0000000000000723
37. Araos J, Kenny JS, Rousseau-Blass F, Pang DS. Dynamic prediction of fluid responsiveness during positive pressure ventilation: a review of the physiology underlying heart-lung interactions and a critical interpretation. Vet Anaesth Analg. (2020) 4:3–14. doi: 10.1016/j.vaa.2019.08.004
38. Silverstein DC, Pruett-Saratan A 2nd, Drobatz KJ. Measurements of microvascular perfusion in healthy anesthetized dogs using orthogonal polarization spectral imaging. J Vet Emerg Crit Care. (2009) 19:579–87. doi: 10.1111/j.1476-4431.2009.00488.x
39. Peruski AM, Cooper ES. Assessment of microcirculatory changes by use of sidestream dark field microscopy during hemorrhagic shock in dogs. Am J Vet Res. (2011) 72:438–745. doi: 10.2460/ajvr.72.4.438
40. Silverstein DC, Cozzi EM, Hopkins AS, Keefe TJ. Microcirculatory effects of intravenous fluid administration in anesthetized dogs undergoing elective ovariohysterectomy. Am J Vet Res. (2014) 75:809–17. doi: 10.2460/ajvr.75.9.809
41. Gommeren K, Allerton FJ, Morin E, Reynaud A, Peeters D, Silverstein DC. Evaluation of a rapid bedside scoring system for microcirculation videos acquired from dogs. J Vet Emerg Crit Care. (2014) 24:554–61. doi: 10.1111/vec.12212
42. Bakker J, Ince C. Monitoring coherence between the macro and microcirculation in septic shock. Curr Opin Crit Care. (2020) 22:729. doi: 10.1097/MCC.0000000000000729
43. Byrne L, Obonyo NG, Diab SD, Dunster KR, Passmore MR, Boon AC, et al. Unintended consequences: fluid resuscitation worsens shock in an ovine model of endotoxemia. Am J Respir Crit Care Med. (2018) 198:1043–54. doi: 10.1164/rccm.201801-0064OC
44. Hahn RG. Adverse effects of crystalloid and colloid fluids. Anaesthesiol Intensive Ther. (2017) 49:303–8. doi: 10.5603/AIT.a2017.0045
45. Malbrain ML, Marik PE, Witters I, Cordemans C, Kirkpatrick AW, Roberts DJ, et al. Fluid overload, de-resuscitation, and outcomes in critically ill or injured patients: a systematic review with suggestions for clinical practice. Anaesthesiol Intensive Ther. (2014) 46:361–80. doi: 10.5603/AIT.2014.0060
46. Cavanagh AA, Sullivan LA, Hansen BD. Retrospective evaluation of fluid overload and relationship to outcome in critically ill dogs. J Vet Emerg Crit Care. (2016) 26:578–86. doi: 10.1111/vec.12477
47. Jacobs R, Jonckheer J, Malbrain MLNG. Fluid overload FADEs away! Time for fluid stewardship. J Crit Care. (2018) 48:458–61. doi: 10.1016/j.jcrc.2018.08.027
48. Ross SW, Christmas AB, Fischer PE, Holway H, Seymour R, Huntington CR, et al. Defining dogma: quantifying crystalloid hemodilution in a prospective randomized control trial with blood donation as a model for hemorrhage. J Am Coll Surg. (2018) 227:321–31. doi: 10.1016/j.jamcollsurg.2018.05.005
49. Van der Linden P, Ickx BE. The effects of colloid solutions on hemostasis. Can J Anaesth. (2006) 53(6 Suppl.):S30–9. doi: 10.1007/BF03022250
50. Dickenmann M, Oettl T, Mihatsch MJ. Osmotic nephrosis: acute kidney injury with accumulation of proximal tubular lysosomes due to administration of exogenous solutes. Am J Kidney Dis. (2008) 51:491–503. doi: 10.1053/j.ajkd.2007.10.044
51. Fenger-Eriksen C, Tønnesen E, Ingerslev J, Sørensen B. Mechanisms of hydroxyethyl starch-induced dilutional coagulopathy. J Thromb Haemost. (2009) 7:1099–105. doi: 10.1111/j.1538-7836.2009.03460.x
52. Kumar AB, Suneja M. Hetastarch-induced osmotic nephrosis. Anesthesiology. (2012) 117:647. doi: 10.1097/ALN.0b013e31824de9ad
53. Gauthier V(1), Holowaychuk MK, Kerr CL, Bersenas AM, Wood RD. Effect of synthetic colloid administration on coagulation in healthy dogs anddogs with systemic inflammation. J Vet Intern Med. (2015) 29:276–85. doi: 10.1111/jvim.12492
54. Bae J, Soliman M, Kim H, Kang S, Kim W, Ahn S, et al. Rapid exacerbation of renal function after administration of hydroxyethyl starch in a dog. J Vet Med Sci. (2017) 79:1591–5. doi: 10.1292/jvms.17-0196
55. Bruno B, Troìa R, Dondi F, Maurella C, Gianella P, Lippi I, et al. Stage 1-biomarkers of kidney injury in dogs undergoing constant rate infusion of hydroxyethyl starch 130/0.4. Animals (Basel). (2021) 11:2555. doi: 10.3390/ani11092555
56. Sigrist NE, Kälin N, Dreyfus A. Effects of hydroxyethyl starch 130/04 on serum creatinine concentration and development of acute kidney injury in nonazotemic cats. J Vet Intern Med. (2017) 31:1749–56. doi: 10.1111/jvim.14813
57. Schmid SM, Cianciolo RE, Drobatz KJ, Sanchez M, Price JM, King LG. Postmortem evaluation of renal tubular vacuolization in critically ill dogs. J Vet Emerg Crit Care. (2019) 29:279–87. doi: 10.1111/vec.12837
58. Trefz FM, Constable PD, Lorenz I. Effect of intravenous small-volume hypertonic sodium bicarbonate, sodium chloride, and glucose solutions in decreasing plasma potassium concentration in hyperkalemic neonatal calves with diarrhea. J Vet Intern Med. (2017) 31:907–21. doi: 10.1111/jvim.14709
59. Wu MC, Liao TY, Lee EM, Chen YS, Hsu WT, Lee MG, et al. Administration of hypertonic solutions for hemorrhagic shock: a systematic review and meta-analysis of clinical trials. Anesth Analg. (2017) 125:1549–57. doi: 10.1213/ANE.0000000000002451
60. Arifianto MR, Ma'ruf AZ, Ibrahim A, Bajamal AH. Role of hypertonic sodium lactate in traumatic brain injury management. Asian J Neurosurg. (2018) 13:971–5. doi: 10.4103/ajns.AJNS_10_17
61. Aydogdu U, Yildiz R, Guzelbektes H, Naseri A, Akyuz E, Sen I. Effect of combinations of intravenous small-volume hypertonic sodium chloride, acetate Ringer, sodium bicarbonate, and lactate Ringer solutions along with oral fluid on the treatment of calf diarrhea. Pol J Vet Sci. (2018) 21:273–80.
62. Millet A, Cuisinier A, Bouzat P, Batandier C, Lemasson B, Stupar V, et al. Hypertonic sodium lactate reverses brain oxygenation and metabolism dysfunction after traumatic brain injury. Br J Anaesth. (2018) 120:1295–303. doi: 10.1016/j.bja.2018.01.025
63. Honore PM, Barreto Gutierrez L, Spapen HD. Renal protection in sepsis: is hypertonic sodium (lactate) the solution? Ann Intensive Care. (2019) 9:28. doi: 10.1186/s13613-019-0505-z
64. Marx G, Meybohm P, Schuerholz T, Lotz G, Ledinko M, Schindler AW, et al. Impact of a new balanced gelatine on electrolytes and pH in the perioperative care. PLoS ONE. (2019) 14:e0213057. doi: 10.1371/journal.pone.0213057
65. Macko A, Sheppard FR, Nugent WH, Abuchowski A, Song BK. Improved hemodynamic recovery and 72-hour survival following low-volume resuscitation with a PEGylated carboxyhemoglobin in a rat model of severe hemorrhagic shock. Mil Med. (2020) 17:usz472. doi: 10.1093/milmed/usz472
66. Caspers M, Maegele M, Fröhlich M. Current strategies for hemostatic control in acute trauma hemorrhage and trauma-induced coagulopathy. Expert Rev Hematol. (2018) 11:987–95. doi: 10.1080/17474086.2018.1548929
67. Osekavage KE, Brainard BM, Lane SL, Almoslem M, Arnold RD, Koenig A. Pharmacokinetics of tranexamic acid in healthy dogs and assessment of its antifibrinolytic properties in canine blood. Am J Vet Res. (2018) 79:1057–63. doi: 10.2460/ajvr.79.10.1057
68. Hickman DA, Pawlowski CL, Shevitz A, et al. Intravenous synthetic platelet (SynthoPlate) nanoconstructs reduce bleeding and improve 'golden hour' survival in a porcine model of traumatic arterial hemorrhage. Sci Rep. (2018) 8:3118. doi: 10.1038/s41598-018-21384-z
69. Li Y, Xiaozhu Z, Guomei R, Qiannan D, Hahn RG. Effects of vasoactive drugs on crystalloid fluid kinetics in septic sheep. PLoS ONE. (2017) 12:e0172361. doi: 10.1371/journal.pone.0172361
70. Chow JH, Abuelkasem E, Sankova S, Henderson RA, Mazzeffi MA, Tanaka KA. Reversal of vasodilatory shock: current perspectives on conventional, rescue, and emerging vasoactive agents for the treatment of shock. Anesth Analg. (2020) 130:15–30. doi: 10.1213/ANE.0000000000004343
71. Haan BJ, Cadiz ML, Natavio AM. Efficacy and safety of vasopressin as first-line treatment of distributive and hemorrhagic shock states. Ann Pharmacother. (2020) 54:213–8. doi: 10.1177/1060028019882035
72. Meresse Z, Medam S, Mathieu C, Duclos G, Vincent JL, Leone M. Vasopressors to treat refractory septic shock: a narrative review. Minerva Anestesiol. (2020) 2020:4. doi: 10.23736/S0375-9393.20.13826-4
73. Finfer S, Myburgh J, Bellomo R. Intravenous fluid therapy in critically ill adults. Nat Rev Nephrol. (2018) 14:717. doi: 10.1038/s41581-018-0044-0
74. de Keijzer IN, Kaufmann T, Scheeren TWL. Which type of fluid to use perioperatively? J Emerg Crit Care Med. (2019) 3:51. doi: 10.21037/jeccm.2019.08.07
75. Perel P, Roberts I, Ker K. Colloids versus crystalloids for fluid resuscitation in critically ill patients. Cochrane Database Syst Rev. (2013) 28:CD000567.pub6. doi: 10.1002/14651858.CD000567.pub6
76. Boer C, Bossers SM, Koning NJ. Choice of fluid type: physiological concepts and perioperative indications. Br J Anaesth. (2018) 120:384–96. doi: 10.1016/j.bja.2017.10.022
77. Mizushima Y, Tohira H, Mizobata Y, Matsuoka T, Yokota J. Fluid resuscitation of trauma patients: how fast is the optimal rate? Am J Emerg Med. (2005) 23:833–7. doi: 10.1016/j.ajem.2005.03.015
78. Roger C, Louart B, Louart G, Bobbia X, Claret PG, Perez-Martin A, et al. Does the infusion rate of fluid affect rapidity of mean arterial pressure restoration during controlled hemorrhage. Am J Emerg Med. (2016) 34:1743–9. doi: 10.1016/j.ajem.2016.05.019
79. Ho L, Lau L, Churilov L, Riedel B, McNicol L, Hahn RG, et al. Comparative evaluation of crystalloid resuscitation rate in a human model of compensated haemorrhagic shock. Shock. (2016) 46:149–57. doi: 10.1097/SHK.0000000000000610
80. Doherty M, Buggy DJ. Intraoperative fluids: how much is too much? Br J Anaesth. (2012) 109:69–79. doi: 10.1093/bja/aes171
81. Marik PE, Byrne L, van Haren F. Fluid resuscitation in sepsis: the great 30 mL per kg hoax. J Thorac Dis. (2020) 12:S37–47. doi: 10.21037/jtd.2019.12.84
82. Meyhoff TS, Møller MH, Hjortrup PB, Cronhjort M, Perner A, Wetterslev J. Lower vs higher fluid volumes during initial management of sepsis: a systematic review with meta-analysis and trial sequential analysis. Chest. (2020) 157:1478–96. doi: 10.1016/j.chest.2019.11.050
83. Hirshberg A, Hoyt DB, Mattox KL. Timing of fluid resuscitation shapes the hemodynamic response to uncontrolled hemorrhage: analysis using dynamic modeling. J Trauma. (2006) 60:1221–7. doi: 10.1097/01.ta.0000220392.36865.fa
84. Kwan I, Bunn F, Chinnock P, Roberts I. Timing and volume of fluid administration for patients with bleeding. Cochrane Database Syst Rev. (2014) 3:CD002245. doi: 10.1002/14651858.CD002245.pub2
85. Feinman M, Cotton BA, Haut ER. Optimal fluid resuscitation in trauma: type, timing, and total. Curr Opin Crit Care. (2014) 20:366–72. doi: 10.1097/MCC.0000000000000104
86. Goodell GM, Campbell J, Hoejvang-Nielsen L, Stansen W, Constable PD. An alkalinizing oral rehydration solution containing lecithin-coated citrus fiber is superior to a nonalkalinizing solution in treating 360 calves with naturally acquired diarrhea. J Dairy Sci. (2012) 95:6677–86. doi: 10.3168/jds.2012-5605
87. Martin GS, Kaufman DA, Marik PE, Shapiro NI, Levett DZH, Whittle J, et al. Perioperative Quality Initiative (POQI) consensus statement on fundamental concepts in perioperative fluid management: fluid responsiveness and venous capacitance. Perioper Med. (2020) 9:12. doi: 10.1186/s13741-020-00142-8
88. Muir WW, Ueyama Y, Noel-Morgan J, Kilborne A, Page J. A. Systematic review of the quality of IV fluid therapy in veterinary medicine. Front Vet Sci. (2017) 4:127. doi: 10.3389/fvets.2017.00127
89. Roberts I, Kwan I, Evans P, Haig S. Does animal experimentation inform human healthcare? Observations from a systematic review of international animal experiments on fluid resuscitation. BMJ. (2002) 324:474–6. doi: 10.1136/bmj.324.7335.474
90. Mapstone J, Roberts I, Evans P. Fluid resuscitation strategies: a systematic review of animal trials. J Trauma. (2003) 55:571–89. doi: 10.1097/01.TA.0000062968.69867.6F
91. Tabbers MM, Boluyt N, Offringa M. Implementation of an evidence-based guideline on fluid resuscitation: lessons learnt for future guidelines. Eur J Pediatr. (2010) 169:749–58. doi: 10.1007/s00431-009-1108-8
92. Yozova ID, Howard J, Sigrist NE, Adamik KN. Current trends in volume replacement therapy and the use of synthetic colloids in small animals-an internet-based survey (2016). Front Vet Sci. (2017) 4:140. doi: 10.3389/fvets.2017.00140
93. Hopper K, Garcia Rojas A, Barter L. An online survey of small animal veterinarians regarding current fluid therapy practices in dogs and cats. J Am Vet Med Assoc. (2018) 252:553–9. doi: 10.2460/javma.252.5.553
94. Hahn RG. Fluid therapy might be more difficult than you think. Anesthesia Analgesia. (2007) 105:304–5. doi: 10.1213/01.ane.0000270218.31147.67
95. Marik PE. Lactate guided resuscitation-nothing is more dangerous than conscientious foolishness. J Thorac Dis. (2019) 15(Suppl.):S1969–72. doi: 10.21037/jtd.2019.07.67
96. Joseph F, Borzelleca. Paracelsus: herald of modern toxicology. Toxicol Sci. (2000) 53:2–4. doi: 10.1093/toxsci/53.1.2
97. Baxter Healthcare Corporation. Lactated Ringers (2000). Available online at: https://www.baxrerpi.com/pi-pdf/Lactated_Ringers_Injection_+viaflex_PI.pdf (accessed April 29, 2020).
98. Rawson RE, Dispensa ME, Goldstein RE, Nicholson KW, Vidal NK. A simulation for teaching the basic and clinical science of fluid therapy. Adv Physiol Educ. (2009) 33:202–8. doi: 10.1152/advan.90211.2008
99. Hoste EA, Maitland K, Brudney CS, Mehta R, Vincent JL, Yates D, et al. ADQI XII Investigators Group. Four phases of intravenous fluid therapy: a conceptual model. Br J Anaesth. (2014) 113:740–7. doi: 10.1093/bja/aeu300
100. Svensén C, Sjöstrand F, Hahn RG. Volume kinetics of intravenous fluid therapy in the prehospital setting. Prehosp Disaster Med. (2001) 16:9–13. doi: 10.1017/S1049023X00025474
101. Bhave G, Neilson EG. Body fluid dynamics: back to the future. J Am Soc Nephrol. (2011) 22:2166–81. doi: 10.1681/ASN.2011080865
102. Carlson GP. Fluid therapy in horses with acute diarrhea. Vet Clin North Am Large Anim Pract. (1979) 1:313–29. doi: 10.1016/S0196-9846(17)30187-8
103. Sutton JD. Digestion and absorption of energy substrates in the lactating cow. J Dairy Sc. (1985) 68:3376–93. doi: 10.3168/jds.S0022-0302(85)81251-0
104. KuKanich B, Coetzee JF, Gehring R, Hubin M. Comparative disposition of pharmacologic markers for cytochrome P-450 mediated metabolism, glomerular filtration rate, and extracellular and total body fluid volume of Greyhound and Beagle dogs. J Vet Pharmacol Ther. (2007) 30:314–9. doi: 10.1111/j.1365-2885.2007.00875.x
105. Gundersen K, Shen G. Total body water in obesity. Am J Clin Nutr. (1955) 19:77–83. doi: 10.1093/ajcn/19.2.77
106. Courtice FC. The blood volume of normal animals. J Physiol. (1943) 102:290–305. doi: 10.1113/jphysiol.1943.sp004035
107. Lindstedt S, Schaeffer P. Use of allometry in predicting anatomical and physiological parameters of mammals. Lab Animals. (2002) 36:1–19. doi: 10.1258/0023677021911731
108. Carlson GP, Bruss M. Fluid, electrolyte, and acid-base balance. In: Kaneko JJ, Harvey JW, Bruss ML, editors, Fluid, Electrolyte, and Acid-Base Balance, Clinical Biochemistry of Domestic Animals. 6th ed. New York, NY: Academic Press (2008). p. 529–59. doi: 10.1016/B978-0-12-370491-7.00017-9
109. Levitt MF, Gaudino AM. Measurement of body water compartments. Am J Med. (1950) 9:208–15. doi: 10.1016/0002-9343(50)90024-6
110. Zdolsek JH, Lisander B, Hahn RG. Measuring the size of the extracellular fluid space using bromide, iohexol, and sodium dilution. Anesth Analg. (2005) 101:1770–7. doi: 10.1213/01.ANE.0000184043.91673.7E
111. Wolf MB. Hemoglobin-dilution method: effect of measurement errors on vascular olume estimation. Comput Math Methods Med. (2017) 2017:3420590. doi: 10.1155/2017/3420590
112. Brandstrup B. Fluid therapy for the surgical patient. Best Pract Res Clin Anaesthesiol. (2006) 20:265–83. doi: 10.1016/j.bpa.2005.10.007
113. Jacob M, Chappell D, Rehm M. The 'third space'–fact or fiction? Best Pract Res Clin Anaesthesiol. (2009) 23:145–57. doi: 10.1016/j.bpa.2009.05.001
114. Ertl AC, Diedrich A, Raj SR. Techniques used for the determination of blood volume. Am J Med Sci. (2007) 334:32–6. doi: 10.1097/MAJ.0b013e318063c6d1
115. Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, oude Egbrink MG. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch. (2007) 454:345–59. doi: 10.1007/s00424-007-0212-8
116. Curry FE. Layer upon layer: the functional consequences of disrupting the glycocalyx-endothelial barrier in vivo and in vitro. Cardiovasc Res. (2017) 113:559–61, doi: 10.1093/cvr/cvx044
117. Jungheinrich C, Neff TA. Pharmacokinetics of hydroxyethyl starch. Clin Pharmacokinet. (2005) 44:681–99. doi: 10.2165/00003088-200544070-00002
118. Vink H, Duling BR. Capillary endothelial surface layer selectively reduces plasma solute distribution volume. Am J Physiol Heart Circ Physiol. (2000) 278:H285–9. doi: 10.1152/ajpheart.2000.278.1.H285
119. Mitra S, Khandelwal P. Are all colloids same? how to select the right colloid? Indian J Anaesth. (2009) 53:592–607. PMID: 20640110.
120. Jiang XZ, Lu Y, Luo KH, Ventikos Y. Understanding endothelial glycocalyx function under flow shear stress from a molecular perspective. Biorheology. (2019) 56:89–100. doi: 10.3233/BIR-180193
121. Chappell D, Jacob M. Role of the glycocalyx in fluid management: small things matter. Best Pract Res Clin Anaesthesiol. (2014) 28:227–34. doi: 10.1016/j.bpa.2014.06.003
122. Birch DJ, Turmaine M, Boulos PB, Burnstock G. Sympathetic innervation of human mesenteric artery and vein. J Vasc Res. (2008) 45:323–32. doi: 10.1159/000119095
123. Gelman S. Venous function and central venous pressure: a physiologic story. Anesthesiology. (2008) 108:735–48. doi: 10.1097/ALN.0b013e3181672607
124. Shen T, Baker K. Venous return and clinical hemodynamics: how the body works during acute hemorrhage. Adv Physiol Educ. (2015) 39:267–71. doi: 10.1152/advan.00050.2015
125. Cannesson M, Jian Z, Chen G, Vu TQ, Hatib F. Effects of phenylephrine on cardiac output and venous return depend on the position of the heart on the Frank-Starling relationship. J Appl Physiol. (1985) 113:281–9. doi: 10.1152/japplphysiol.00126.2012
126. Jacobs R, Lochy S, Malbrain MLNG. Phenylephrine-induced recruitable preload from the venous side. J Clin Monit Comput. (2019) 33:373–6. doi: 10.1007/s10877-018-0225-1
127. Guyton AC, Lindsey AW, Abernathy B, Richardson T. Venous return at various right atrial pressures and the normal venous return curve. Am J Physiol. (1957) 189:609–15. doi: 10.1152/ajplegacy.1957.189.3.609
128. Magder S. Volume and its relationship to cardiac output and venous return. Crit Care. (2016) 20:271. doi: 10.1186/s13054-016-1438-7
129. Levy MN. The cardiac and vascular factors that determine systemic blood flow. Circ Res. (1979) 44:739–47. doi: 10.1161/01.RES.44.6.739
130. Rothe CF. Reflex controls of veins and vascular capacitance. Physiol Rev. (1983) 63:1281–341. doi: 10.1152/physrev.1983.63.4.1281
131. Tyberg JV. How changes in venous capacitance modulate cardiac output. Pflugers Arch. (2002) 445:10–7. doi: 10.1007/s00424-002-0922-x
132. Reddi BA, Carpenter RH. Venous excess: a new approach to cardiovascular control and its teaching. J Appl Physiol. (2005) 98:356–64. doi: 10.1152/japplphysiol.00535.2004
133. Beard DA, Feigl EO. Understanding Guyton's venous return curves. Am J Physiol Heart Circ Physiol. (2011) 30:H629–33. doi: 10.1152/ajpheart.00228.2011
134. Brengelmann GL A. critical analysis of the view that right atrial pressure determines venous return. J Appl Physiol. (2003) 94:849–59. doi: 10.1152/japplphysiol.00868.2002
135. Brengelmann GL. Venous return and the physical connection between distribution of segmental pressures and volumes. Am J Physiol Heart Circ Physiol. (2019) 317:H939–53. doi: 10.1152/ajpheart.00381.2019
136. Dalmau R. Venous return: a fresh start. Am J Physiol Heart Circ Physiol. (2019) 317:H1102–4. doi: 10.1152/ajpheart.00575.2019
137. Akram M, Hamid A. A comprehensive review on water balance. Biomed Nutr. (2013) 3:193–5. doi: 10.1016/j.bionut.2012.10.003
138. Olsson K. Fluid balance in ruminants: adaptation to external and internal challenges. Ann N Y Acad Sci. (2005) 1040:156–61. doi: 10.1196/annals.1327.020
139. Patel VB, Zhong JC, Grant MB, Oudit GY. Role of the ACE2/angiotensin 1-7 axis of the renin-angiotensin system in heart failure. Circ Res. (2016) 118:1313–26. doi: 10.1161/CIRCRESAHA.116.307708
140. Knepper MA, Kwon TH, Nielsen S. Molecular physiology of water balance. N Engl J Med. (2015) 373:196. doi: 10.1056/NEJMc1505505
141. Bie P. Natriuretic peptides and normal body fluid regulation. Compr Physiol. (2018) 8:1211–49. doi: 10.1002/cphy.c180002
142. Bie P. Mechanisms of sodium balance: total body sodium, surrogate variables, and renal sodium excretion. Am J Physiol Regul Integr Comp Physiol. (2018) 315:R945–62. doi: 10.1152/ajpregu.00363.2017
143. Delpire E, Gagnon KB. Water homeostasis and cell volume maintenance and regulation. Curr Top Membr. (2018) 81:3–52. doi: 10.1016/bs.ctm.2018.08.001
144. Sugie J, Intaglietta M, Sung LA. Water transport and homeostasis as a major function of erythrocytes. Am J Physiol Heart Circ Physiol. (2018) 314:H1098–107. doi: 10.1152/ajpheart.00263.2017
145. Bankir L, Bouby N, Trinh-Trang-Tan MM. The role of the kidney in the maintenance of water balance. Baillieres Clin Endocrinol Metab. (1989) 3:249–311. doi: 10.1016/S0950-351X(89)80005-9
146. Ellison D, Farrar FC. Kidney influence on fluid and electrolyte balance. Nurs Clin North Am. (2018) 53:469–80. doi: 10.1016/j.cnur.2018.05.004
147. Dunn A, Lo V, Donnelly S. The role of the kidney in blood volume regulation: the kidney as a regulator of the hematocrit. Am J Med Sci. (2007) 334:65–71. doi: 10.1097/MAJ.0b013e318095a4ae
148. Jacob M, Saller T, Chappell D, Rehm M, Welsch U, Becker BF. Physiological levels of A-, B- and C-type natriuretic peptide shed the endothelial glycocalyx and enhance vascular permeability. Basic Res Cardiol. (2013) 108:347. doi: 10.1007/s00395-013-0347-z
149. Wiig H, Rubin K, Reed RK. New and active role of the interstitium in control of interstitial fluid pressure: potential therapeutic consequences. Acta Anesthesiol Scand. (2003) 47:111–21. doi: 10.1034/j.1399-6576.2003.00050.x
150. Gavaghan M. Cardiac anatomy and physiology: a review. AORN J. (1998) 67:802–22. doi: 10.1016/S0001-2092(06)62644-6
151. Reed RK, Rubin K. Transcapillary exchange: role and importance of the interstitial fluid pressure and the extracellular matrix. Cardiovasc Res. (2010) 8:211–7. doi: 10.1093/cvr/cvq143
152. Suresh K, Shimoda LA. Lung circulation. Compr Physiol. (2016) 6:897–943. doi: 10.1002/cphy.c140049
153. Moore JE Jr, Bertram CD. Lymphatic system flows. Annu Rev Fluid Mech. (2018) 50:459–82. doi: 10.1146/annurev-fluid-122316-045259
154. Nakada T, Kwee IL. Fluid dynamics inside the brain barrier: current concept of interstitial flow, glymphatic flow, and cerebrospinal fluid circulation in the brain. Neuroscientist. (2019) 25:155–66. doi: 10.1177/1073858418775027
155. Curry FR, Adamson RH. Vascular permeability modulation at the cell, microvessel, or whole organ level: towards closing gaps in our knowledge. Cardiovasc Res. (2010) 87:218–29. doi: 10.1093/cvr/cvq115
156. Frank BW, Kern F Jr. Intestinal and liver lymph and lymphatics. Gastroenterology. (1968) 55:408–22. doi: 10.1016/S0016-5085(19)34052-1
157. Tuma PL, Hubbard AL. Transcytosis: crossing cellular barriers. Physiol Rev. (2003) 83:871–932. doi: 10.1152/physrev.00001.2003
158. Pillinger NL, Kam P. Endothelial glycocalyx: basic science and clinical implications. Anaesth Intensive Care. (2017) 45:295–307. doi: 10.1177/0310057X1704500305
159. Jacob M, Bruegger D, Rehm M, Welsch U, Conzen P, Becker BF. Contrasting effects of colloid and crystalloid resuscitation fluids on cardiac vascular permeability. Anesthesiology. (2006) 104:1223–31. doi: 10.1097/00000542-200606000-00018
160. Sarin H. Physiologic upper limits of pore size of different blood capillary types and another perspective on the dual pore theory of microvascular permeability. J Angiogenes Res. (2010) 2:14. doi: 10.1186/2040-2384-2-14
161. Danziger J, Zeidel ML. Osmotic homeostasis. Clin J Am Soc Nephrol. (2015) 10:852–62. doi: 10.2215/CJN.10741013
162. Roumelioti ME, Glew RH, Khitan ZJ, Rondon-Berrios H, Argyropoulos CP, Malhotra D, et al. Fluid balance concepts in medicine: principles and practice. World J Nephrol. (2018) 7:1–28. doi: 10.5527/wjn.v7.i1.1
163. Weiskopf RB, James MF. Update of use of hydroxyethyl starches in surgery and trauma. J Trauma Acute Care Surg. (2015) 78:S54–S9. doi: 10.1097/TA.0000000000000636
164. He H, Liu D, Ince C. Colloids and the microcirculation. Anesth Analg. (2018) 126:1747–54. doi: 10.1213/ANE.0000000000002620
165. Michel CC, Curry FE. Microvascular permeability. Physiol Rev. (1999) 79:703–61. doi: 10.1152/physrev.1999.79.3.703
166. Curry FE. The molecular structure of the endothelial glycocalyx layer (EGL) and surface layers (ESL) modulation of transvascular exchange. Adv Exp Med Biol. (2018) 1097:29–49. doi: 10.1007/978-3-319-96445-4_2
167. Choi PT, Yip G, Quinonez LG, Cook DJ. Crystalloids vs. colloids in fluid resuscitation: a systematic review. Crit Care Med. (1999) 27:200–10. doi: 10.1097/00003246-199901000-00053
168. Raghunathan K, Murray PT, Beattie WS, Lobo FN, Myburg J, Sladen R, et al. Choice of fluid in acute illness: what should be given? An international consensus. Br J Anaesth. (2014) 113:772–83. doi: 10.1093/bja/aeu301
169. Zaar M, Lauritzen B, Secher NH, Krantz T, Nielsen HB, Madsen PL, et al. Initial administration of hydroxyethyl starch vs lactated Ringer after liver trauma in the pig. Br J Anaesth. (2009) 102:221–6. doi: 10.1093/bja/aen350
170. Hartog CS, Bauer M, Reinhart K. The efficacy and safety of colloid resuscitation in the critically ill. Anesth Analg. (2011) 112:156–64. doi: 10.1213/ANE.0b013e3181eaff91
171. Jacob M, Chappell D, Hofmann-Kiefer K, Helfen T, Schuelke A, Jacob B, et al. The intravascular volume effect of Ringer's lactate is below 20%: a prospective study in humans. Crit Care. (2012) 16:R86. doi: 10.1186/cc11344
172. Orbegozo Cortés D, Gamarano Barros T, Njimi H, Vincent J-L. Crystalloids versus colloids. Anesthesia Analgesia. (2015) 120:389–402. doi: 10.1213/ANE.0000000000000564
173. Finfer S, Bellomo R, Boyce N, French J, Myburgh J, Norton R, et al. comparison of albumin and saline for fluid resuscitation in the intensive care unit. N Engl J Med. (2004) 350:2247–56. doi: 10.1056/NEJMoa040232
174. Hahn RG. Why are crystalloid and colloid fluid requirements similar during surgery and intensive care? Eur J Anaesthesiol. (2013) 30:515–8. doi: 10.1097/EJA.0b013e328362a5a9
175. László I, Demeter G, Öveges N, Érces D, Kaszaki J, Tánczos K, et al. Volume-replacement ratio for crystalloids and colloids during bleeding and resuscitation: an animal experiment. Intensive Care Med Exp. (2017) 5:52. doi: 10.1186/s40635-017-0165-y
176. Fodor GH, Habre W, Balogh AL, Südy R, Babik B, Peták F. Optimal crystalloid volume ratio for blood replacement for maintaining hemodynamic stability and lung function: an experimental randomized controlled study. BMC Anesthesiol. (2019) 19:21. doi: 10.1186/s12871-019-0691-0
177. Passmore MR, Obonyo NG, Byrne L, Boon AC, Diab SD, Dunster KR, et al. Fluid resuscitation with 0.9% saline alters haemostasis in an ovine model of endotoxemic shock. Thromb Res. (2019) 176:39–45. doi: 10.1016/j.thromres.2019.02.015
178. Ziebart A, Ruemmler R, Möllmann C, Kamuf J, Garcia-Bardon A, Thal SC, et al. Fluid resuscitation-related coagulation impairment in a porcine hemorrhagic shock model. PeerJ. (2020) 8:e8399. doi: 10.7717/peerj.8399
179. Hahn RG, Lyons G. The half-life of infusion fluids: an educational review. Eur J Anaesthesiol. (2016) 33:475–82. doi: 10.1097/EJA.0000000000000436
180. Starling EH. On the absorption of fluids from the connective tissue spaces. J Physiol. (1896) 19:312–26. doi: 10.1113/jphysiol.1896.sp000596
181. Axel L. Flow limits of Kedem-Katchalsky equations for fluid flux. Bull Math Biol. (1976) 38:671–7. doi: 10.1016/S0092-8240(76)80007-9
182. Landis EM. The relationship between capillary pressure and the rate at which fluid passes through the walls of single capillaries. Am J Physiol. (1927) 82:217–38. doi: 10.1152/ajplegacy.1927.82.2.217
183. Landis EM. Factors controlling the movement of fluid through the human capillary wall yale. J Biol Med. (1933) 5:201–25.
184. Pappenheimer JR, Soto-Rivera A. Effective osmotic pressure of the plasma proteins and other quantities associated with the capillary circulation in the hind limb of cats and dogs. Am J Physiol. (1948) 152:471–449. doi: 10.1152/ajplegacy.1948.152.3.471
185. Popel AS, Johnson PC. Microcirculation and hemorheology. Annu Rev Fluid Mech. (2005) 37:43–69. doi: 10.1146/annurev.fluid.37.042604.133933
186. Taylor AE. Capillary fluid filtration. Starling forces and lymph flow. Circ Res. (1981) 49:557–75. doi: 10.1161/01.RES.49.3.557
187. Staverman AJ. The theory of measurement of osmotic pressure. Recueil des Travaux Chimiques des Pays-Bas. (1951) 70:344–52. doi: 10.1002/recl.19510700409
188. Levick JR. Revision of the Starling principle: new views of tissue fluid balance. J Physiol. (2004) 557:704. doi: 10.1113/jphysiol.2004.066118
189. Michel CC. Starling: the formulation of his hypothesis of microvascular fluid exchange and its significance after 100 years. Exp Physiol. (1997) 82:1–30. doi: 10.1113/expphysiol.1997.sp004000
190. Weinbaum S, Tsay R, Curry FE. A three-dimensional junction-pore-matrix model for capillary permeability. Microvasc Res. (1992) 44:85–111. doi: 10.1016/0026-2862(92)90104-W
191. Hu X, Adamson RH, Liu B, Curry FE, Weinbaum S. Starling forces that oppose filtration after tissue oncotic pressure is increased. Am J Physiol Heart Circ Physiol. (2000) 279:H1724–36. doi: 10.1152/ajpheart.2000.279.4.H1724
192. Adamson RH. Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J Physiol. (2004) 557:889–907. doi: 10.1113/jphysiol.2003.058255
193. Curry FE, Adamson RH. Endothelial glycocalyx: permeability barrier and mechanosensor. Ann Biomed Eng. (2012) 40:828–39. doi: 10.1007/s10439-011-0429-8
194. Thind GS, Zanders S, Baker JK. Recent advances in the understanding of endothelial barrier function and fluid therapy. Postgrad Med J. (2018) 94:289–95. doi: 10.1136/postgradmedj-2017-135125
195. Guerci P, Ergin B, Uz Z, Ince Y, Westphal M, Heger M, et al. Glycocalyx degradation is independent of vascular barrier permeability increase in nontraumatic hemorrhagic shock in rats. Anesth Analg. (2019) 129:598–607. doi: 10.1213/ANE.0000000000003918
196. Dull RO, Hahn RG. Transcapillary refill: the physiology underlying fluid reabsorption. J Trauma Acute Care Surg. (2021). F90:e31–9. doi: 10.1097/TA.0000000000003013
197. Arnemann PH, Hessler M, Kampmeier T, Seidel L, Malek Y, Van Aken H, et al. Resuscitation with hydroxyethyl starch maintains hemodynamic coherence in ovine hemorrhagic shock. Anesthesiology. (2020) 132:131–9. doi: 10.1097/ALN.0000000000002998
198. Svensen CH, Rodhe PM, Prough DS. Pharmacokinetic aspects of fluid therapy. Best Pract Res Clin Anaesthesiol. (2009) 23:213–24. doi: 10.1016/j.bpa.2008.11.003
199. Svensén CH, Brauer KP, Hahn RG, Uchida T, Traber LD, Traber DL, Prough DS. Elimination rate constant describing clearance of infused fluid from plasma is independent of large infusion volumes of 09% saline in sheep. Anesthesiology. (2004) 101:666–74. doi: 10.1097/00000542-200409000-00015
200. Silverstein DC, Aldrich J, Haskins SC, Drobatz KF, Cowgill LD. Assessment of changes in blood volume in response to resuscitative fluid administration in dogs. J Vet Emerg Crit Care. (2005) 15:185–92. doi: 10.1111/j.1476-4431.2005.00138.x
201. Woodcock TE. Plasma volume, tissue oedema, and the steady-state Starling principle. BJA Education. (2017) 17:74–8. doi: 10.1093/bjaed/mkw035
202. Hirshberg A, Hoyt DB, Mattox KL. From “leaky buckets” to vascular injuries: understanding models of uncontrolled hemorrhage. J Am Coll Surg. (2007) 204:665–72. doi: 10.1016/j.jamcollsurg.2007.01.005
203. Hahn RG, Drobin D, Zdolsek J. Distribution of crystalloid fluid changes with the rate of infusion: a population-based study. Acta Anaesthesiol Scand. (2016) 60:569–78. doi: 10.1111/aas.12686
204. Valverde A, Gianotti G, Rioja-Garcia E, Hathway A. Effects of high-volume, rapid-fluid therapy on cardiovascular function and hematological values during isoflurane-induced hypotension in healthy dogs. Can J Vet Res. (2012) 76:99–108.
205. Lambden S, Creagh-Brown BC, Hunt J. Definitions and pathophysiology of vasoplegic shock. Crit Care. (2018) 22:174. doi: 10.1186/s13054-018-2102-1
206. Levy B, Fritz C, Tahon E. Vasoplegia treatments: the past, the present, and the future. Crit Care. (2018) 22:174. doi: 10.1186/s13054-018-1967-3
207. Van der Linden P, De Hert S, Mathieu N, Degroote F, Schmartz D, Zhang H, et al. Tolerance to acute isovolemic hemodilution. Effect of anesthetic depth. Anesthesiology. (2003) 99:97–104. doi: 10.1097/00000542-200307000-00018
208. Morita Y, Chin-Yee I, Yu P, Sibbald WJ, Martin CM. Critical oxygen delivery in conscious septic rats under stagnant or anemic hypoxia. Am J Respir Crit Care Med. (2003) 167:868–72. doi: 10.1164/rccm.200205-490OC
209. Pape A, Kutschker S, Kertscho H, Stein P, Horn O, Lossen M, et al. The choice of the intravenous fluid influences the tolerance of acute normovolemic anemia in anesthetized domestic pigs. Crit Care. (2012) 16:R69. doi: 10.1186/cc11324
210. Connolly CM, Kramer GC, Hahn RG, Chaisson NF, Svensén CH, Kirschner RA, et al. Isoflurane but not mechanical ventilation promotes extravascular fluid accumulation during crystalloid volume loading. Anesthesiology. (2003) 98:670–81. doi: 10.1097/00000542-200303000-00015
211. Marik P. The physiology of fluid resuscitation. Curr Anesthesiol Rep. (2014) 4:353–9. doi: 10.1007/s40140-014-0080-7
212. Hahn RG, Nemme J. Volume kinetic analysis of fluid retention after induction of general anesthesia. BMC Anesthesiol. (2020) 20:95. doi: 10.1186/s12871-020-01001-1
213. Boscan P, Pypendop BH, Siao KT, Francey T, Dowers K, Cowgill L, et al. Fluid balance, glomerular filtration rate, and urine output in dogs anesthetized for an orthopedic surgical procedure. Am J Vet Res. (2010) 71:501–7. doi: 10.2460/ajvr.71.5.501
214. Egan ED, Johnson KB. The influence of hemorrhagic shock on the disposition and effects of intravenous anesthetics: a narrative review. Anesth Analg. (2020) 130:1320–30. doi: 10.1213/ANE.0000000000004654
215. Gelman S, Mushlin PS. Catecholamine-induced changes in the splanchnic circulation affecting systemic hemodynamics. Anesthesiology. (2004) 100:434–43. doi: 10.1097/00000542-200402000-00036
216. Vane LA, Prough DS, Kinsky MA, Williams CA, Grady JJ, Kramer GC. Effects of different catecholamines on the dynamics of volume expansion of crystalloid infusion. Anesthesiology. (2004) 101:1136–44. doi: 10.1097/00000542-200411000-00013
217. Ewaldsson CA, Vane LA, Kramer GC, Hahn RG. Adrenergic drugs alter both the fluid kinetics and the hemodynamic responses to volume expansion in sheep. J Surg Res. (2006) 131:7–14. doi: 10.1016/j.jss.2005.09.012
218. Stephens CT, Uwaydah N, Kramer GC, Prough DS, Salter M, Kinsky MP. Vascular and extravascular volume expansion of dobutamine and norepinephrine in normovolemic sheep. Shock. (2011) 36:303–11. doi: 10.1097/SHK.0b013e318225b031
219. Asmussen S, Salter M, Prough DS, Kramer GC, Svensen C, Sheffield-Moore M, et al. Isoproternenol increases vascular volume expansion and urinary output after a large crystalloid bolus in healthy volunteers. Shock. (2014) 42:407–714. doi: 10.1097/SHK.0000000000000233
220. Kaneko T, Tatara T, Hirose M. Effects of anaesthesia-induced hypotension and phenylephrine on plasma volume expansion by hydroxyethyl starch: a randomised controlled study. Acta Anaesthesiol Scand. (2020) 64:620–7. doi: 10.1111/aas.13548
221. Tatara T, Tsunetoh T, Tashiro C. Crystalloid infusion rate during fluid resuscitation from acute haemorrhage. Br J Anaesth. (2007) 99:212–7. doi: 10.1093/bja/aem165
222. Ogbu OC, Murphy DJ, Martin GS. How to avoid fluid overload. Curr Opin Crit Care. (2015) 21:315–21. doi: 10.1097/MCC.0000000000000211
223. Santry HP, Alam HB. Fluid resuscitation: past, present, and the future. Shock. (2010) 33:229–41. doi: 10.1097/SHK.0b013e3181c30f0c
224. Naumann DN, Beaven A, Dretzke J, Hutchings S, Midwinter MJ. Searching for the optimal fluid to restore microcirculatory flow dynamics after haemorrhagic shock: a systematic review of preclinical studies. Shock. (2016) 46:609–22. doi: 10.1097/SHK.0000000000000687
225. MacDonald N, Pearse RM. Are we close to the ideal intravenous fluid? Br J Anaesth. (2017) 119(Suppl.1):i63–i71. doi: 10.1093/bja/aex293
226. Muir W. Effect of intravenously administered crystalloid solutions on acid-base balance in domestic animals. J Vet Intern Med. (2017) 31:1371–81. doi: 10.1111/jvim.14803
227. Zwager CL, Tuinman PR, de Grooth HJ. Why physiology will continue to guide the choice between balanced crystalloids and normal saline: a systematic review and meta-analysis. Crit Care. (2019) 23:366. doi: 10.1186/s13054-019-2658-4
228. Williams AT, Lucas A, Muller CR, Bolden-Rush C, Palmer AF, Cabrales P. Balance between oxygen transport and blood rheology during resuscitation from hemorrhagic shock with polymerized bovine hemoglobin. J Appl Physiol. (1985). (2020) 129:97–107. doi: 10.1152/japplphysiol.00016.2020
229. Johansson PI, Stensballe J, Ostrowski SR. Shock induced endotheliopathy (SHINE) in acute critical illness - a unifying pathophysiologic mechanism. Crit Care. (2017) 21:25. doi: 10.1186/s13054-017-1605-5
230. Black JA, Pierce VS, Juneja K, Holcomb JB. Complications of hemorrhagic shock and massive transfusion-a comparison before and after the damage control resuscitation era. Shock. (2021) 56:42–51. doi: 10.1097/SHK.0000000000001676
231. Holcomb JB, Tilley BC, Baraniuk S, Fox EE, Wade CE, Podbielski JM, et al. PROPPR Study Group. Transfusion of plasma, platelets, and red blood cells in a 1:1:1 vs a 1:1:2 ratio and mortality in patients with severe trauma: the PROPPR randomized clinical trial. J Am Med Assoc. (2015) 313:471–82. doi: 10.1001/jama.2015.12
232. Bogert JN, Harvin JA, Cotton BA. Damage control resuscitation. J Intensive Care Med. (2016) 31:177–86. doi: 10.1177/0885066614558018
233. Sheppard FR, Schaub LJ, Cap AP, Macko AR, Moore HB, Moore EE, et al. Whole blood mitigates the acute coagulopathy of trauma and avoids the coagulopathy of crystalloid resuscitation. J Trauma Acute Care Surg. (2018) 85:1055–62. doi: 10.1097/TA.0000000000002046
234. Guyette FX, Sperry JL, Peitzman AB, Billiar TR, Daley BJ, Miller RS, et al. Prehospital blood product and crystalloid resuscitation in the severely injured patient: a secondary analysis of the prehospital air medical plasma trial. Ann Surg. (2021) 273:358–64. doi: 10.1097/SLA.0000000000003324
235. Chong MA, Wang Y, Berbenetz NM, McConachie I. Does goal-directed haemodynamic and fluid therapy improve peri-operative outcomes? A systematic review and meta-analysis. Eur J Anaesthesiol. (2018) 35:469–83. doi: 10.1097/EJA.0000000000000778
236. Jiang S, Wu M, Lu X, Zhong Y, Kang X, Song Y, Fan Z. Is restrictive fluid resuscitation beneficial not only for hemorrhagic shock but also for septic shock? a meta-analysis. Medicine. (2021) 100:e25143. doi: 10.1097/MD.0000000000025143
237. Pfortmueller CA, Schefold JC. Hypertonic saline in critical illness -a systematic review. J Crit Care. (2017) 42:168–77. doi: 10.1016/j.jcrc.2017.06.019
238. Wodicka JR, Chambers AM, Sangha GS, Goergen CJ, Panitch A. Development of a glycosaminoglycan derived, selectin targeting anti-adhesive coating to treat endothelial cell dysfunction. Pharmaceuticals. (2017) 10:36. doi: 10.3390/ph10020036
239. Dekker NAM, van Meurs M, van Leeuwen ALI, Hofland HM, van Slyke P, Vonk ABA, et al. Vasculotide, an angiopoietin-1 mimetic, reduces pulmonary vascular leakage and preserves microcirculatory perfusion during cardiopulmonary bypass in rats. Br J Anaesth. (2018) 121:1041–51. doi: 10.1016/j.bja.2018.05.049
240. Uchimido R, Schmidt EP, Shapiro NI. The glycocalyx: a novel diagnostic and therapeutic target in sepsis. Crit Care. (2019) 23:16. doi: 10.1186/s13054-018-2292-6
241. Ferenz KB, Steinbicker AU. Artificial oxygen carriers-past, present, and future-a review of the most innovative and clinically relevant concepts. J Pharmacol Exp Ther. (2019) 369:300–10. doi: 10.1124/jpet.118.254664
242. Sen Gupta A. Hemoglobin-based oxygen carriers: current state-of-the-art and novel molecules. Shock. (2019) 52:70–83. doi: 10.1097/SHK.0000000000001009
243. Siegemund M, Hollinger A, Gebhard EC, Scheuzger JD, Bolliger D. The value of volume substitution in patients with septic and haemorrhagic shock with respect to the microcirculation. Swiss Med Wkly. (2019) 149:w20007. doi: 10.4414/smw.2019.20007
244. Oller L, Dyer WB, Santamaría L, Largo C, Javidroozi M, Shander A. The effect of a novel intravenous fluid (Oxsealife®) on recovery from haemorrhagic shock in pigs. Anaesthesia. (2019) 74:765–77. doi: 10.1111/anae.14627
245. Milford EM, Reade MC. Resuscitation fluid choices to preserve the endothelial glycocalyx. Crit Care. (2019) 23:77. doi: 10.1186/s13054-019-2369-x
246. Endo Y, Kawase K, Miyasho T, Sano T, Yamashita K, Muir WW. Plethysmography variability index for prediction of fluid responsiveness during graded haemorrhage and transfusion in sevoflurane-anaesthetized mechanically ventilated dogs. Vet Anaesth Analg. (2017) 44:1303–12. doi: 10.1016/j.vaa.2017.07.007
247. Endo Y, Tamura J, Ishizuka T, Itami T, Hanazono K, Miyoshi K, et al. Stroke volume variation (SVV) and pulse pressure variation (PPV) as indicators of fluid responsiveness in sevoflurane anesthetized mechanically ventilated euvolemic dogs. J Vet Med Sci. (2017) 79:1437–45. doi: 10.1292/jvms.16-0287
248. Sano H, Chambers JP. Ability of pulse wave transit time to detect changes in stroke volume and to estimate cardiac output compared to thermodilution technique in isoflurane-anaesthetised dogs. Vet Anaesth Analg. (2017) 44:1057–67. doi: 10.1016/j.vaa.2016.11.014
249. Chan A, Hughes D, Tennent-Brown BS, Boller M. In vitro effects of lactated Ringer's solution, hypertonic saline, hydroxyethyl starch, hypertonic saline/hydroxyethyl starch, and mannitol on thromboelastographic variables of canine whole blood. J Vet Emerg Crit Care. (2020) 30:264–71. doi: 10.1111/vec.12929
250. Yaguiyan-Colliard L, Daumas C, Nguyen P, Grandjean D, Cardot P, Priymenko N, et al. Evaluation of total body water in canine breeds by single-frequency bioelectrical impedance analysis method: specific equations are needed for accuracy. BMC Res Notes. (2015) 8:336. doi: 10.1186/s13104-015-1298-2
251. Latman NS, Keith N, Nicholson A, Davis M. Bioelectrical impedance analysis determination of water content and distribution in the horse. Res Vet Sci. (2011) 90:516–20. doi: 10.1016/j.rvsc.2010.07.012
252. Miller A, Mandeville J. Predicting and measuring fluid responsiveness with echocardiography. Echo Res Pract. (2016) 3:G1–12. doi: 10.1530/ERP-16-0008
253. Desai ND. Garry D. Assessing dynamic fluid-responsiveness using transthoracic echocardiography in intensive care. BJA Educ. (2018) 18: 218e226. doi: 10.1016/j.bjae.2018.03.005
254. Moon YJ, Moon HS, Kim DS. Deep learning-based stroke volume estimation outperforms conventional arterial contour method in patients with hemodynamic instability. J Clin Med. (2019) 8:1419. doi: 10.3390/jcm8091419
255. Rinehart J, Lilot M, Lee C. Closed-loop assisted versus manual goal-directed fluid therapy during high-risk abdominal surgery: a case-control study with propensity matching. Crit Care. (2015) 19:94. doi: 10.1186/s13054-015-0827-7
256. Dave S, Shriyan D, Gujjar P. Newer drug delivery systems in anesthesia. J Anaesthesiol Clin Pharmacol. (2017) 33:157–63. doi: 10.4103/joacp.JOACP_63_16
257. Hundeshagen G, Kramer GC, Ribeiro Marques N, Salter MG, Koutrouvelis AK Li H, et al. Closed-loop- and decision-assist-guided fluid therapy of human hemorrhage. Crit Care Med. (2017) 45:e1068–74. doi: 10.1097/CCM.0000000000002593
258. Uemura K, Kawada T, Zheng C, Li M, Sugimachi M. Computer-controlled closed-loop drug infusion system for automated hemodynamic resuscitation in endotoxin-induced shock. BMC Anesthesiol. (2017) 17:145. doi: 10.1186/s12871-017-0437-9
259. Gholami B, Haddad WM, Bailey JM, Geist B, Ueyama Y, Muir WW, et al. pilot study evaluating adaptive closed-loop fluid resuscitation during states of absolute and relative hypovolemia in dogs. J Vet Emerg Crit Care. (2018) 28:436–46. doi: 10.1111/vec.12753
Keywords: physiology, fluid compartments, perfusion, volume kinetics, monitoring, novel fluids
Citation: Muir WW, Hughes D and Silverstein DC (2021) Editorial: Fluid Therapy in Animals: Physiologic Principles and Contemporary Fluid Resuscitation Considerations. Front. Vet. Sci. 8:744080. doi: 10.3389/fvets.2021.744080
Received: 19 July 2021; Accepted: 21 September 2021;
Published: 20 October 2021.
Edited and reviewed by: Mujeeb Ur Rehman, Livestock and Dairy Development Department, Pakistan
Copyright © 2021 Muir, Hughes and Silverstein. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: William W. Muir, bW9ub3MzNjkmI3gwMDA0MDtnbWFpbC5jb20=; d2lsbGlhbS5tdWlyJiN4MDAwNDA7bG11bmV0LmVkdQ==
†These authors have contributed equally to this work and share first authorship