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Research Article

The Use of Crystalloidal and Colloidal Solutions for Volume Replacement in Hypovolemic Shock

Pages 1-26 | Published online: 27 Sep 2008

References

  • Graham T. Liquid diffusion applied to analysis. Philos. Trans. R. Soc. London 1861; 151: 183
  • Pfeffer W. Osmotische Untersuchungen. Studien zur Zellemechanik. Englemann, Leipzig 1877
  • van t'Hoff J. H. Die Rolle des osmotischen Druckes in der Analogie Zwischen Lösungen und Gasen. Z. Phys. Chem. Stoechiom. Verwandschaftsl. 1887; 481
  • Starling E. H. On the absorption of fluids from the connective tissue spaces. J. Physiol. (London) 1896; 19: 312
  • Starling E. H. Production and absorption of lymph. Textbook of Physiology, E. A. Schaefer. Caxton, London 1898; Vol 1: 285
  • Crile G. W. An Experimental Research into Surgical Shock. Lippincott, Philadelphia 1899
  • Mann F. C. The peripheral origin of surgical shock. Johns Hopkins Hasp. Bull 1914; 25: 205
  • Courtice F. C. The development of concepts of fluid balance. Edema, N. C. Staub, A. E. Taylor. Raven Press, New York 1984; 1
  • Ward G. Transfusion of plasma. Br. Med. J. 1918; 1: 301
  • Bayliss W. M. Intravenous Injection in Wound Shock. Longmans, Green, London 1918
  • Cournand A., Noble R. P., Breed E. S., Lauson H. D., Baldwin E. D. F., Pinchot G. B., Richards D. W., Jr. Chemical, clinical, and immunologic studies on the product of human plasma fractionation. VIII. Clinical use of concentrated human serum albumin in shock, and comparison with whole blood and with rapid saline infusion. J. Clin. Invest. 1944; 23: 491
  • Strumia M. The development of plasma preparations for transfusions. Ann. Int. Med. 1941; 80: 80
  • Graham J., Buckwalter J., Hartley J., Brinkhous K. Canine hemophilia: observations on the course, the clotting anomaly, and the effect of blood transfusions. J. Exp. Med. 1949; 90: 97
  • Tullis J. L. Albumin Background and use. JAMA 1977; 237: 355
  • Sgouris J. T., Dorsey H. W. Survey of the use of plasma expanders in the United States. Proc. Workshop on Albumin, J. T. Sgouris, A. Rene. U.S. Government Printing Office, Washington, D.C 1975; 137
  • Skillman J. J. The role of albumin and oncotically active fluids in shock. Crit. Care Med. 1976; 4: 55
  • Boutros A. Intra- and postoperative use of albumin. Curr. Stud. Hematol. Blood Transf. 1986; 53: 180
  • Haupt M. T. Colloidal and crystalloidal fluid resuscitation in shock associated with increased capillary permeability. Curr. Stud. Hematol. Blood Transfus. 1986; 53: 86
  • Granger D. N., Gabel J. C., Drake R. E., Taylor A. E. Physiologic basis for the clinical use of albumin solutions. Surg. Gynecol. Obstet. 1978; 146: 97
  • Shires T., Collins D., Carrico J., Lightfoot S. Fluid therapy in hemorrhagic shock. Surg. Forum. 1960; 11: 115
  • Annari F. T. Serum osmolality: uses and limitations. N. Engl. J. Med. 1984; 310: 102
  • Guyton A. C. Transport through the cell membrane. Textbook of Medical Physiology, A. C Guyton. W. B. Saunders, Philadelphia 1986; 88
  • Andreoli T. E. Osmolality distrubances. Cecil Textbook of Medicine, J. B. Wyngaarden, L. H. Smith. W. B. Saunders, Philadelphia 1985; 523
  • Pitts R. F. Volume and composition of the body fluids. Physiology of the Kidney and Body Fluids. Year Book Medical Publishers, Chicago 1974; 11
  • Pappenheimer J. R., Soto-Rivera A. Effective osmotic pressure of the plasma proteins and other quantities associated with the capillary circulation in the hind limbs of cats and dogs. Am. J. Physiol. 1948; 152: 471
  • Staverman A. J. The theory of measurement of osmotic pressure. Recl. Trav. Chim. Pays Bos 1951; 70: 344
  • Kedem O., Katchalsky A. Thermodynamic analysis of the permeability of biologial membranes and electrolytes. Biochim. Biophys. Acta 1958; 27: 229
  • Carlson R. W., Schaeffer R. C, Jr, Michaels S. G., Weil M. H. Pulmonary edema fluid: spectrum of features in 37 patients. Circulation 1979; 60: 1161
  • Landis E. M. Capillary pressure and capillary permeability. Physiol. Rev. 1934; 14: 404
  • Guyton A. C. Capillary dynamics and exchange of fluid between the blood and interstitial fluid. Textbook of Medical Physiology;, A. C Guyton. W. B. Saunders, Philadelphia 1986; 348
  • Granger H. J., Laine G. A., Barnes G. E., Lewis R. E. Dynamics and control of transmicrovascular fluid exchange. Edema, N. D. Staub, A. E. Taylor. New York, Raven Press 1984; 189
  • Wiederhielm C. A., Woodbury J. W., Kirk S., Rushmer R. F. Pulsatile pressue in the microcirculation of the frog's mesentery. Am. J. Physiol. 1964; 207: 173
  • Pappenheimer J. R., Soto-Rivera A. Effective osmotic pressure of the plasma proteins and other quantities associated with the capillary circulation of the hindlimb of cats and dogs. Am. J. Physiol. 1948; 152: 471
  • Johnson P. C. Effect of venous pressure on mean capillary pressure and vascular resistance in the intestine. Circ. Res. 1965; 16: 294
  • Granger H. J., Barnes G. E., Chen H. I. Transcapillary fluid balance in canine skeletal muscle during graded venous hypertension. Fed. Proc. Fed. Am. Soc. Exp. Biol. 1981; 40: 45
  • Wiedemann H. P., Matthay M. A., Matthay R. A. I. Cardiovascular pulmonary monitoring in the Intensive Care Unit. Chest 1984; 85: 537
  • Urbach D. R., Rippe J. M. Pulmonary artery catheter placement and care. Intensive Care Medicine, J. M. Rippe, R. S. Irwin, J. S. Alpert, J. E. Dalen. Boston, Little, Brown 1985
  • Holloway H., Perry M., Downey J., Parker J., Taylor A. Estimation of effective pulmonary capillary pressure in intact lungs. J. Appl. Physiol. 1983; 54: 846
  • Parker R. E., Granger D. N., Taylor A. E. Estimates of isogravimetric capillary presures during alveolar hypoxia. Am. J. Physiol. 1981; 241: H732
  • Hakim T. S., Dawson C. A., Linehan J. H. Hemodynamic responses of dog lung lobe to lobar venous occlusion. J. Appl. Physiol. 1979; 47: 145
  • Linehan J. H., Dawson C. A., Rickaby D. A. Distribution of vascular resistance and compliance in a dog lung lobe. J. Appl. Physiol. 1982; 53: 158
  • Weil M. H., Shubin H. The “VIP” approach to the bedside management of shock. JAMA 1969; 207: 337
  • Starchuck E., Weil M. H., Shubin H. Fluid challenge. Critical Care Medicine Handbook, M. H. Weil, H. Shubin. John N. Kolen, New York 1974
  • Constadt S. N., Thys D., Mindich B. P., Kaplan J. A., Goldman M. Validation of quantitative intraoperative transesophageal echocardiography. Anesthesiology 1986; 65: 418
  • Urbanowicz J. H., Cohen N. H. Is transesophageal echocardiography a measure of left ventricular function?. Anesthesiology 1987; 66: 586
  • Orloff M. J., Bell R. H. Long term survival of emergency portacaval shunting for bleeding varices in patients with alcoholic cirrhosis. Am. J. Surg. 1986; 151: 176
  • Reynolds T. B., Ito S., Iwatsuki S. Measurement of portal pressure and its clinical application. Am. J. Med. 1970; 49: 649
  • Atkinson M., Sherlock S. Intrasplenic pressure as an index of portal venous pressure. Lancet 1954; 1: 1325
  • Boyer T. D., Triger D. R., Horisawa M., Redeken A. G., Reynolds T. B. Direct transhepatic measurement of portal vein pressure using a thin needle. Comparison with wedged hepatic vein pressure. Gastroenterology 1977; 72: 584
  • Weil M. H., Michaels S., Puri V. K., Carlson R. W. The stat laboratory. Facilitating blood gas and biochemical measurements for the critically ill and injured. Am. J. Clin. Pathol. 1981; 76: 34
  • Rackow E. C, Fein L. A., Leppo J. Colloid osmotic pressure as a prognostic indicator of pulmonary edema and mortality in the critically ill. Chest 1977; 72: 709
  • Bisera J., Weil M. H., Michaels S., Bernardo A., Stein B. An “oncometer” for clinical measurement of colloid osmotic pressue of plasma. Clin. Chem. 1978; 24: 1586
  • Ladegaar-Pederson H. J. Measurement of the colloid osmotic pressure in patients. Scand. J. Clin. Lab. Invest. 1967; 20: 79
  • Intaglietta M., Zweifach B. W. Measurement of blood plasma colloid osmotic pressure. 1. Technical aspects. II. Comparative study of different species. Microvasc. Res. 1971; 3: 72
  • Rowe M. I., Lankau C, Newmark S. Clinical evaluation of methods to monitor colloid oncotic pressure in the surgical treatment of children. Surg. Gynecol. Obstet. 1974; 139: 889
  • Landes E. M., Pappenheimer J. R. Exchange of substances through capillary walls. Handbook of Physiology, Vol. 2, Circulation, Section 2, W. F. Hamilton, Phillip Dow. American Physiological Society, Bethesda, MD 1963
  • Blantz R.C., Konnen K. S., Tucker B. J. Glomerular filtration response to elevated ureteral pressure in both the hydropenic and the plasma expanded rat. Circ. Res. 1975; 37: 819
  • Will B. R., Brace R. A. Physiological effects of pH changes on colloid osmotic pressures. Am. J. Physiol. 1985; 248: H890
  • Haupt M. T., Rackow E. C. Colloid osmotic pressure and fluid resuscitation with hetastarch, albumin, and saline solutions. Crit. Care Med. 1982; 10: 159
  • Dawidson I., Gelin L., Haglind E. Plasma volume, intravascular protein content, hemodynamic and oxygen transport changes during intestinal shock in dogs. Crit. Care Med. 1980; 8: 73
  • Brigham K. L., Snell J. D., Harris T. R., Marshall S., Haynes J., Bowers R. E., Perry J. Indicator dilution lung water and vascular permeability in humans. Circ. Res. 1979; 44: 523
  • da Luz P. L., Shubin H., Weil M. H., Jacobson E., Stein L. Pulmonary edema related to changes in colloid osmotic and pulmonary artery wedge pressure in patients after acute myocardial infarction. Circulation 1975; 52: 350
  • Rackow E. C, Fein I. A, Siegel J. The relationships of the colloid osmotic pulmonary artery wedge pressure gradient to pulmonary edema and mortality in critically ill patients. Chest 1982; 82: 433
  • Carlson R. W., Haupt M. T. Colloid-hydrostatic gradients and pulmonary edema. Chest 1982; 83: 399
  • Comper W. D. Interstitium. Edema, N. D. Staub, A. E. Taylor. Raven Press, New York 1984; 229
  • Comper W. D., Laurent T. C. Physiological function of connective tissue polysaccharides. Physiol. Rev. 1978; 58: 225
  • Deno D.C., Saba T. M., Lewis E. P. Kinetics of endogenously labelled plasma fibronectin: incorporation into tissues. Am. J. Physiol. 1983; 254: R564
  • Guyton A. C. The lymphatic system, interstitial fluid dynamics, edema, and pulmonary fluid. Textbook of Medical Physiology, A. C Guyton. W. B. Saunders, Philadelphia 1986; 361
  • Demling R. H. Shock and fluids. Critical Care State of the Art. Society of Critical Care Medicine, Fullerton, CA 1986; Vol. 7: 301
  • Guyton A. C., Coleman T. G. Regulation of interstitial fluid volume and pressure. Ann. N. Y. Acad. Sci. 1968; 150: 537
  • Mawhinney H. J. D., Roddie I. C. Spontaneous activity on bovine mesenteric lymphatics. J. Physiol. (London) 1973; 229: 339
  • Smith R. O. Lymphatic contractility. A possible intrinsic mechanism of lymphatic vessels on the transport of lymph. J. Exp. Med. 1948; 90: 497
  • Kramer G.C., Gunther R. A., Nerlich M. L., Zweifach S. S., Demling R. R. Effect of dextran-70 on increased microvascular fluid and protein flux after thermal injury. Circ. Shock 1982; 9: 529
  • Staub N. C. Pathogenesis of pulmonary edema. Am. Rev. Respir. Dis. 1974; 109: 358
  • Taylor A. E., Gibson W. H., Granger H. J., Guyton A. C. The interaction between intracapillary and tissue forces in the overall regulation of interstitial fluid volume. Lymphology 1973; 6: 192
  • Granger D. N., Mortillaro N. A., Taylor A. E. Interactions of analysis of intestinal lymph flow and “secretion”. Am. J. Physiol. 1977; 232: 13
  • Olszewski W. L., Engeset A., Sokolowski J. Lymph flow and protein in the normal male leg during lying, getting up, and walking. Lymphology 1977; 10: 178
  • Parker J.C., Perry M. A., Taylor A. E. Permeability of the microvascular barrier. Edema, N. C. Staub, A. E. Taylor. Raven Press, New York 1984; 143
  • Felgenhawer K. Protein size and cerebrospinal fluid composition. Klin. Wochenschr. 1974; 52: 1158
  • Pappenheimer J. R. Passage of molecules through capillary walls. Physiol. Rev. 1953; 33: 387
  • Palade G. E. Fine structure of blood capillaries. J. Appl. Phys. 1953; 24: 1424
  • Renkin E. M. Capillary transport of macromolecules: pores and other endothelial pathways. J. Appl. Physiol. 1985; 58: 315
  • Gil J. Roles of plasmalemmal vesicles in cells: a multidisciplinary approach. Fed. Proc. Fed. Am. Exp. Biol 1983; 42: 2406
  • Simionescu M., Simionescu N. Function of the endothelial cell surface. Ann. Rev. Physiol. 1986; 48: 273
  • Simionescu M., Ghitescu L., Fixman A., Simionescu N. How plasma macromolecules cross the endothelium. NIPS 1987; 2: 97
  • Schneeberger E., Hamelin M. Interaction of serum proteins with lung endothelial glycocalyx: its effect on capillary permeability. Am. J. Physiol. 1984; 247: 206
  • Curr F. E. Effect of albumin on the structure of the molecular filter of the capillary wall. Fed. Proc. Fed. Am. Soc. Exp. Biol. 1985; 44: 2610
  • Ryan U. S. The endothelial surface and responses to injury. Fed. Proc. Fed. Am. Soc. Exp. Biol. 1986; 45: 101
  • Majno G., Palade G. E. Studies on inflammation. II. The effect of histamine and serotonin on vascular permeability. An electron microscopic study. J. Biophys. Biochem. Cytol. 1961; 11: 571
  • Cotran R. S., Suter E. R., Majno G. The use of colloidal carbon as a tracer for vascular injury. A review. Vasc. Dis. 1961; 4: 571
  • Hurley J. V. Acute inflammation: the effect of concurrent leukocyte migration and increased permeability on particle retention by the vascular wall. Br. J. Exp. Pathol. 1964; 45: 627
  • Parker J., Martin D., Rutile G. Prevention of free radical mediated vascular permeabiltiy increase in lung using superoxide-dismutase. Chest 1983; 83: 525
  • Fox R., Fox W. Dimethylsulfoxide prevents hydroxyl radical mediated depolymerization of hyaluronic acid. Ann. N. Y. Acad. Sci. 1983; 411: 14
  • Linder E. Binding of Clq and complement activation by vascular endothelium. J. Immunol. 1981; 126: 648
  • Linder E., Leito V. P., Stenman S. Activation of complement by cytoskeletal intermediate filaments. Nature (London) 1979; 278: 176
  • Till G. O., Johnson K. J., Kunkel R., Ward P. A. Intravascular activation of complement and acute lung injury. Dependence of neutrophils and toxic oxygen metabolites. Clin. Invest. 1982; 69: 1126
  • Grega G. J., Svensjo E. Pharmacology of water and macromolecular permeability in the forelimb of the dog. Edema, N. C. Staub, A. E. Taylor. Raven Press, New York 1984; 405
  • Gibbon J. H., Jr. Experimental pulmonary edema following lobectomy and plasma infusion. Surgery 1942; 12: 694
  • Hultgren H. N. High altitude pulmonary edema. Lung, Water, and Solute Exchange, N. C Staub. Dekker, New York 1978; 437
  • Theodore J., Robin E. D. Speculations on neurogenic pulmonary edema. Am. Rev. Rspir. Dis. 1976; 113: 405
  • Landolt C.C., Matthay M. A., Albertine K. H., Roos P. J., Wiener-Kronish J. P., Staub N. C. Overperfusion, hypoxia, and increased pressure cause only hydrostatic pulmonary edema in anesthetized sheep. Circ. Res. 1983; 52: 335
  • Carter R. D., Joyner W. L., Renkin E. M. Effects of histamine and some other substances on molecular selectivity of the capillary wall to plasma proteins and dextran. Microvasc. Res. 1974; 7: 31
  • Joyner W. L. Effect of prostaglandins on macromolecular transport from blood to lymph in the dog. Am. J. Physiol. 1977; 236: H690
  • Joyner W. L., Carter R. D., Raizes G. S., Renkin E. M. Influence of histamine and some other substances on blood-lymph transport of plasma protein and dextran in the dog paw. Microvasc. Res. 1974; 7: 19
  • Robin E. D., Carey L. C., Grenvik A., Glauser F., Gaudio R. Capillary leak syndrome with pulmonary edema. Arch. Intern. Med. 1972; 130: 66
  • Marty A. T. Hyperoncotic albumin therapy. Surg. Gynecol. Obstet. 1974; 139: 105
  • Oratz M. Oncotic pressure and albumin synthesis. Plasma Protein Metabolism, M. A. Rothschild, T. Waldman. Academic Press, New York 1970; 223
  • Siegel D.C., Cochin A., Geocaris T., Moss G. S. Effects of saline and colloid resuscitation on renal function. Ann. Surg. 1973; 177: 51
  • Lucas C. E., Weaver D., Higgin R. F., Ledgerwood A. M., Johnson S. D., Bouwman D. L. Effects of albumin versus non-albumin resuscitation on plasma volume and renal excretary function. J. Trauma 1978; 18: 564
  • Shires G. T., Canizaro P. C. Fluid resuscitation in the severely injured. Surg. Clin. North Am. 1973; 53: 1341
  • Monafo W. W., Halverson J. D., Schechtman K. The role of concentrated sodium solutions in the resuscitation of patients with severe burns. Surgery 1984; 95: 129
  • Eliakim M., Rosenberg S., Braum K. Effect of hypertonic saline on the pulmonary and systemic pressures. Circ. Res. 1958; 6: 357
  • Kravath R. E., Aharon A. S., Abal G., Finberg L. Clinically significant physiologic danger from rapidly administered hypertonic poisoning: acute osmol poisoning. Pediatrics 1970; 46: 267
  • Finberg L. Hypernatremic (hypertonic) dehydration in infants. N. Engl. J. Med. 1973; 289: 196
  • Lucas C. E., Ledgerwood A. M., Mammen E. F. Altered coagulation protein content after albumin resuscitation. Ann. Surg. 1982; 196: 198
  • Shoemaker W.C., Bryan-Brown C. W., Quigley L., Stahr L., Elwyn O. H. Body fluid shifts in depletion and post-stress states and then correction with adequate nutrition. Surg. Gynecol. Obstet. 1973; 136: 371
  • Hauser C. J., Shoemaker W. C., Turpin I., Goldberg S. J. Oxygen transport responses to colloid and crystalloid in critically ill surgical patients. Surg. Gynecol. Obstet. 1980; 150: 811
  • Moss G. Postoperative metabolism. The role of plasma albumin in the enteral absorption of water and electrolytes. Pacif. Med. Surg. 1967; 75: 355
  • Thompson W. L. Rational use of albumin and plasma substitutes. Johns Hopkins Med. J. 1975; 136: 220
  • Bland J. H. L., Laver M. B., Lowenstein E. Vasodilator effect of commercial 5% plasma protein fraction solutions. JAMA 1973; 224: 1721
  • Boon J.C., Jesch F., Ring J., Messmer K. Longterm intravascular persistence of hydroxyethylstarch (HES) in man. Eur. Surg. Res. 1976; 8: 497
  • Thompson W. L. Hydroxyethylstarch. Blood Substitutes and Plasma Expanders. Alan R. Liss, New York 1978
  • Atik M. Dextra 40 and Dextran 70: a review. Arch. Surg. 1967; 94: 664
  • Rackow E.C., Faik J. L., Fein I. A., Siegel J. S., Packman M. I., Haupt M. T., Kaufman B. S., Putnam D. Fluid resuscitation in circulatory shock: a comparison of the cardiorespiratory effects of albumin, hetastarch, and saline solutions in patients with hypovolemic and septic shock. Crit. Care Med. 1983; 11: 835
  • Monafo W. W., Wachtel T. L., Dietz F. Bioassay of hemorrhagic shock in rats. Arch. Surg. 1969; 98: 275
  • Haupt M. T., Teerapong P., Green D., SchaefTer R. C, Carlson R. W. Increased pulmonary edema with crystalloid compared to colloid resuscitation of shock associated with increased vascular permeability. Circ. Shock 1984; 12: 213
  • Jing D. L., Kohler J. P., Rice C. L., Moss G. S. Albumin therapy in pulmonary edema. J. Surg. Res. 1982; 3: 482
  • Prewitt R. M., McCarthy J., Wood L. D. H. Treatment of acute low pressure pulmonary edema in dogs. J. Clin. Invest. 1981; 67: 409
  • SchaefTer R.C., Bamhart M. I., Carlson R. W. Pulmonary fibrin deposition and increased microvascular permeability to protein following fibrin microembolism in dogs: a structure-function relationship. Microvasc. Res. 1984; 33: 327
  • SchaefTer R.C., Reniewicz B. A., Chilton S. M., Carlson R. W. Effects of colloid or crystalloid solutions on edemagenesis in normal and thrombomicroembolized lungs. Crit. Care Med. 1987; 15: 1110
  • Risenberg B., Webb W. R., Osbum K., Pilgreen K., Wax S. D., Moulder P. V. Pulmonary microvascular leakage after microembolization and hemodilution. Surgery 1982; 92: 409
  • Finch J. S., Reid C, Bandy K., Fickle D. Compared effects of selected colloids on extravascular lung water in dogs after oleic acid-induced lung injury and severe hemorrhage. Crit. Care Med. 1983; 11: 267
  • Metildi L. A., Schackford S. R., Virgilio R. W., Peters R. M. Crystalloid versus colloid in fluid resuscitation of patients with severe pulmonary insufficiency. Surg. Gynecol. Obstet. 1984; 158: 207
  • Boutros A. R., Ruess R., Olson L., Hoyt J. L., Baker W. H. Comparison of hemodynamic, pulmonary, and renal effects of use of three types of fluids after major surgical procedures on the abdominal aorta. Crit. Care Med. 1979; 7: 9
  • Shires G. T., Peitzman A. B., Albert S. A., Illness H., Silane M. F., Perry M. O., Ghires G. T. Response of extravascular lung water to intraoperative fluids. Ann. Surg. 1983; 197: 515
  • Virgilio R. W., Rice C. L., Smith D. E., James D. R., Zarins C. K., Hobelmann C. F., Peters R. M. Crystalloid vs. colloid resuscitation: is one better?. Surgery 1979; 85: 129
  • Siegel D.C., Cochin A., Geocaris T., Moss G. S. Effects of saline and colloid resuscitation on renal function. Ann. Surg. 1973; 177: 51
  • Moran M., Kaspner C. Acute renal failure associated with elevated plasma oncotic pressure. N. Engl. J. Med. 1987; 317: 150
  • Hunt T. K., Twomey P., Zederfeldt B., Dunphy J. E. Respiratory gas exchange tensions and pH in healing wounds. Am. J. Surg. 1967; 114: 302
  • Hengan C, Niinikoski J., Hunt T. K. Effect of excessive infusion of saline solution on tissue oxygen transport. Surg. Gynecol. Obstet. 1972; 135: 257
  • Remensnyder J. P. Topography of tissue oxygen changes in acute bum edema. Arch. Surg. 1972; 105: 477
  • Mangalore P., Hunt T. K. Effect of varying oxygen tension on healing of open wounds. Surg. Gynecol. Obstet. 1972; 135: 756

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