Analyze Diet
The Journal of physiology2013; 591(18); 4499-4513; doi: 10.1113/jphysiol.2013.257956

Acetazolamide attenuates transvascular fluid flux in equine lungs during intense exercise.

Abstract:   During intense exercise in horses the transvascular fluid flux in the pulmonary circulation (Jv-a) represents 4% of cardiac output (Q). This fluid flux has been attributed to an increase in pulmonary transmural hydrostatic forces, increases in perfused microvascular surface area, and reversible alterations in capillary permeability under conditions of high flow and pressure. Erythrocyte fluid efflux, however, accounts for a significant fraction of Jv-a. In the lung the Jacobs-Stewart cycle occurs with diffusion of CO2 into alveolar space with possible accompanying chloride (Cl-) and water movement from the erythrocyte directly into the pulmonary interstitium. We hypothesised that inhibition of carbonic anhydrase in erythrocytes inhibits the Jacobs-Stewart cycle and attenuates Jv-a. Five horses were exercised on a treadmill until fatigue without (control) and with acetazolamide treatment (30 mg kg(-1) 30 min before exercise). Erythrocyte fluid efflux, plasma fluid flux across the lung and Jv-a were calculated using haemoglobin, haematocrit, plasma protein and Q. Fluid fluxes were used to calculate erythrocyte, plasma and whole blood Cl- fluxes across the lung. Cardiac output was not different between control and acetazolamide treatment. During exercise erythrocyte fluid efflux and Jv-a increased in control (9.3±3.3 and 11.0±4.4 l min(-1), respectively) and was higher than after acetazolamide treatment (3.8±1.6 and 1.2±1.2 l min(-1), respectively) (P<0.05). Plasma fluid flux did not change from rest in control and decreased after acetazolamide treatment (-4.5±1.5 l min(-1)) (P<0.05). Erythrocyte Cl- flux increased during exercise in control and after acetazolamide treatment (P<0.05). During exercise plasma Cl- flux across the lung did not change in control; however, it increased with acetazolamide treatment (P=0.0001). During exercise whole blood Cl- flux increased across the lung in control (P<0.05) but not after acetazolamide treatment. The results indicate that Jv-a in the lung is dependent on the Jacobs-Stewart cycle and mostly independent of transmural hydrostatic forces. It also appears that Jv-a is mediated by Cl- and water egress from erythrocytes directly into the interstitium without transit through plasma.
Publication Date: 2013-07-01 PubMed ID: 23818694PubMed Central: PMC3784195DOI: 10.1113/jphysiol.2013.257956Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research study investigates the influence of Acetazolamide on the transvascular fluid flux within the lungs of horses during strenuous exercise. The study concludes that Acetazolamide effectively reduces the fluid flux in horses, and indicates that the flux is influenced by the Jacobs-Stewart cycle rather than by transmural hydrostatic forces.

Background

  • The study’s premise is a phenomenon observed in horses where intense physical activity increases fluid flux across the transvascular system in the lungs.
  • This fluid exchange amounts to 4% of the animal’s cardiac output and is believed to be due to an increase in pulmonary transmural hydrostatic forces, an increase in the perfused microvascular surface area, and reversible variations in capillary permeability under conditions of high blood flow and pressure.
  • Of the mechanisms contributing to this fluid flux, fluid efflux from erythrocytes is significant.
  • The Jacobs-Stewart cycle, which is the process of carbon dioxide diffusing into the alveolar space with possible associated chloride and water movement from the erythrocytes to the pulmonary interstitium, takes place in the lung.

Objective and Hypotheses

  • The study aims to understand whether inhibiting carbonic anhydrase in erythrocytes, which effectively inhibits the Jacobs-Stewart cycle, can reduce fluid flux.
  • The researchers hypothesize that Acetazolamide, a carbonic anhydrase inhibitor, can attenuate the fluid flux during intense exercise in horses.

Methodology and Findings

  • The study involved five horses who were subjected to strenuous exercise on a treadmill till they reached fatigue, both with and without Acetazolamide treatment.
  • Biological markers such as hemoglobin, hematocrit, plasma protein, and cardiac output were used to calculate erythrocyte fluid efflux, plasma fluid flux across the lung, and the overall fluid flux.
  • The research findings showed that fluid efflux and overall fluid flux increased during exercise in the control group but was significantly less in the group that received Acetazolamide treatment.
  • However, chloride flux from erythrocytes recorded an increase during exercise in both the control group and the Acetazolamide treatment group.
  • While plasma chloride flux did not change during exercise in the control group, it increased considerably in the group subjected to Acetazolamide treatment. Chloride flux in whole blood escalated across the lung in the control group during exercise, whereas it remained unchanged after Acetazolamide treatment.

Conclusion

  • The findings suggest that the fluid flux, indicated by the variable Jv-a, relies on the Jacobs-Stewart cycle and is relatively independent of transmural hydrostatic forces, contrary to previous assumptions.
  • The study also proposes that the fluid flux is mediated by chloride and water egress from erythrocytes directly into the interstitium, not involving plasma transit.
  • Effectively, the study concludes that the administration of Acetazolamide can attenuate the fluid flux in horse lungs during intense physical exertion and provides a new understanding of the mechanisms behind this fluid exchange phenomenon.

Cite This Article

APA
Vengust M, Staempfli H, Viel L, Swenson ER, Heigenhauser G. (2013). Acetazolamide attenuates transvascular fluid flux in equine lungs during intense exercise. J Physiol, 591(18), 4499-4513. https://doi.org/10.1113/jphysiol.2013.257956

Publication

ISSN: 1469-7793
NlmUniqueID: 0266262
Country: England
Language: English
Volume: 591
Issue: 18
Pages: 4499-4513

Researcher Affiliations

Vengust, Modest
  • M. Vengust: University in Ljubljana, Veterinary Faculty, Ljubljana SI-1115, PO Box 3425, Slovenia. modest.vengust@vf.uni-lj.si.
Staempfli, Henry
    Viel, Laurent
      Swenson, Erik R
        Heigenhauser, George

          MeSH Terms

          • Acetazolamide / pharmacology
          • Animals
          • Carbon Dioxide / blood
          • Carbonic Anhydrase Inhibitors / pharmacology
          • Chlorides / blood
          • Erythrocytes / drug effects
          • Erythrocytes / metabolism
          • Hematocrit
          • Horses
          • Lung / drug effects
          • Lung / metabolism
          • Lung / physiology
          • Physical Exertion
          • Pulmonary Circulation / drug effects
          • Pulmonary Gas Exchange

          Grant Funding

          • Canadian Institutes of Health Research

          References

          This article includes 62 references
          1. Alberts MK, Clarke CR, MacAllister CG, Homer LM. Pharmacokinetics of acetazolimide after intravenous and oral administration in horses.. Am J Vet Res 2000 Aug;61(8):965-8.
            pubmed: 10951991doi: 10.2460/ajvr.2000.61.965google scholar: lookup
          2. Bai C, Fukuda N, Song Y, Ma T, Matthay MA, Verkman AS. Lung fluid transport in aquaporin-1 and aquaporin-4 knockout mice.. J Clin Invest 1999 Feb;103(4):555-61.
            pmc: PMC408096pubmed: 10021464doi: 10.1172/jci4138google scholar: lookup
          3. Balanos GM, Talbot NP, Dorrington KL, Robbins PA. Human pulmonary vascular response to 4 h of hypercapnia and hypocapnia measured using Doppler echocardiography.. J Appl Physiol (1985) 2003 Apr;94(4):1543-51.
          4. Bhattacharya J. Hydraulic conductivity of lung venules determined by split-drop technique.. J Appl Physiol (1985) 1988 Jun;64(6):2562-7.
            pubmed: 3403440doi: 10.1152/jappl.1988.64.6.2562google scholar: lookup
          5. Bretscher MS. A major protein which spans the human erythrocyte membrane.. J Mol Biol 1971 Jul 28;59(2):351-7.
            pubmed: 5566420doi: 10.1016/0022-2836(71)90055-6google scholar: lookup
          6. Buono MJ, Yeager JE. Intraerythrocyte and plasma lactate concentrations during exercise in humans.. Eur J Appl Physiol Occup Physiol 1986;55(3):326-9.
            pubmed: 3732260doi: 10.1007/bf02343807google scholar: lookup
          7. Cardenas V Jr, Heming TA, Bidani A. Kinetics of CO2 excretion and intravascular pH disequilibria during carbonic anhydrase inhibition.. J Appl Physiol (1985) 1998 Feb;84(2):683-94.
            pubmed: 9475881doi: 10.1152/jappl.1998.84.2.683google scholar: lookup
          8. Chow EI, Crandall ED, Forster RE. Kinetics of bicarbonate-chloride exchange across the human red blood cell membrane.. J Gen Physiol 1976 Dec;68(6):633-52.
            pmc: PMC2228450pubmed: 993774doi: 10.1085/jgp.68.6.633google scholar: lookup
          9. Coates G, O'Brodovich H, Jefferies AL, Gray GW. Effects of exercise on lung lymph flow in sheep and goats during normoxia and hypoxia.. J Clin Invest 1984 Jul;74(1):133-41.
            pmc: PMC425193pubmed: 6736245doi: 10.1172/jci111393google scholar: lookup
          10. Costill DL, Branam L, Eddy D, Fink W. Alterations in red cell volume following exercise and dehydration.. J Appl Physiol 1974 Dec;37(6):912-6.
            pubmed: 4436223doi: 10.1152/jappl.1974.37.6.912google scholar: lookup
          11. Cousin JL, Motais R, Sola F. Transmembrane exchange of chloride with bicarbonate ion in mammalian red blood cells: evidence for a sulphonamide-sensitive "carrier".. J Physiol 1975 Dec;253(2):385-99.
          12. Crandall ED, Mathew SJ, Fleischer RS, Winter HI, Bidani A. Effects of inhibition of RBC HCO3-/Cl- exchange on CO2 excretion and downstream pH disequilibrium in isolated rat lungs.. J Clin Invest 1981 Oct;68(4):853-62.
            pmc: PMC370872pubmed: 6793631doi: 10.1172/jci110340google scholar: lookup
          13. Dempsey JA, Wagner PD. Exercise-induced arterial hypoxemia.. J Appl Physiol (1985) 1999 Dec;87(6):1997-2006.
            pubmed: 10601141doi: 10.1152/jappl.1999.87.6.1997google scholar: lookup
          14. Dill DB, Costill DL. Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration.. J Appl Physiol 1974 Aug;37(2):247-8.
            pubmed: 4850854doi: 10.1152/jappl.1974.37.2.247google scholar: lookup
          15. Endeward V, Musa-Aziz R, Cooper GJ, Chen LM, Pelletier MF, Virkki LV, Supuran CT, King LS, Boron WF, Gros G. Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane.. FASEB J 2006 Oct;20(12):1974-81.
            pubmed: 17012249doi: 10.1096/fj.04-3300comgoogle scholar: lookup
          16. Endeward V, Cartron JP, Ripoche P, Gros G. RhAG protein of the Rhesus complex is a CO2 channel in the human red cell membrane.. FASEB J 2008 Jan;22(1):64-73.
            pubmed: 17712059doi: 10.1096/fj.07-9097comgoogle scholar: lookup
          17. Erickson BK, Erickson HH, Coffman JR. Pulmonary artery, aortic and oesophageal pressure changes during high intensity treadmill exercise in the horse: a possible relation to exercise-induced pulmonary haemorrhage.. Equine Vet J Suppl 1990 Jun;(9):47-52.
          18. Gordon JB, Rehorst-Paea LA, Hoffman GM, Nelin LD. Pulmonary vascular responses during acute and sustained respiratory alkalosis or acidosis in intact newborn piglets.. Pediatr Res 1999 Dec;46(6):735-41.
          19. Hamburger H. Uber der Einfluss der Athmung auf die Permeabilitit der Blutkörperchen. Biochem Z 1891;28:405.
          20. Hamburger H. Anionenwanderungen in Serum und Blut unter dem Einfluss von CO2, Saure und Akali. Biochem Z 1918;86:309–324.
          21. HANSEN AT. Osmotic pressure effect of the red blood cells--possible physiological significance.. Nature 1961 May 6;190:504-8.
            pubmed: 13711314doi: 10.1038/190504a0google scholar: lookup
          22. Hodgson DR, Rose RJ, McCutcheon LJ, Kelso TB, Bayly WM, Gollnick PD. Effects of acetazolamide on cardiorespiratory and metabolic responses to submaximal exercise. Equine Exercise Physiol 1991;3:343–352.
          23. Höhne C, Pickerodt PA, Francis RC, Boemke W, Swenson ER. Pulmonary vasodilation by acetazolamide during hypoxia is unrelated to carbonic anhydrase inhibition.. Am J Physiol Lung Cell Mol Physiol 2007 Jan;292(1):L178-84.
            pubmed: 16936246doi: 10.1152/ajplung.00205.2006google scholar: lookup
          24. Jackson EK. Diuretics. Goodman & Gilman's The Pharmacological Basis of Therapeutics 1996;9th edn. New York: McGraw-Hill; pp. 691–695.
          25. Jacobs MH, Stewart DR. THE ROLE OF CARBONIC ANHYDRASE IN CERTAIN IONIC EXCHANGES INVOLVING THE ERYTHROCYTE.. J Gen Physiol 1942 Mar 20;25(4):539-52.
            pmc: PMC2142531pubmed: 19873294doi: 10.1085/jgp.25.4.539google scholar: lookup
          26. Jonk AM, van den Berg IP, Olfert IM, Wray DW, Arai T, Hopkins SR, Wagner PD. Effect of acetazolamide on pulmonary and muscle gas exchange during normoxic and hypoxic exercise.. J Physiol 2007 Mar 15;579(Pt 3):909-21.
          27. Kifor G, Toon MR, Janoshazi A, Solomon AK. Interaction between red cell membrane band 3 and cytosolic carbonic anhydrase.. J Membr Biol 1993 Jun;134(3):169-79.
            pubmed: 8411120doi: 10.1007/bf00234498google scholar: lookup
          28. Kowalchuk JM, Heigenhauser GJ, Sutton JR, Jones NL. Effect of acetazolamide on gas exchange and acid-base control after maximal exercise.. J Appl Physiol (1985) 1992 Jan;72(1):278-87.
            pubmed: 1537726doi: 10.1152/jappl.1992.72.1.278google scholar: lookup
          29. Kowalchuk JM, Heigenhauser GJ, Sutton JR, Jones NL. Effect of chronic acetazolamide administration on gas exchange and acid-base control after maximal exercise.. J Appl Physiol (1985) 1994 Mar;76(3):1211-9.
            pubmed: 8005865doi: 10.1152/jappl.1994.76.3.1211google scholar: lookup
          30. Lloyd TC Jr. Influence of blood pH on hypoxic pulmonary vasoconstriction.. J Appl Physiol 1966 Mar;21(2):358-64.
            pubmed: 5934435doi: 10.1152/jappl.1966.21.2.358google scholar: lookup
          31. Ma B, Xiang Y, Mu SM, Li T, Yu HM, Li XJ. Effects of acetazolamide and anordiol on osmotic water permeability in AQP1-cRNA injected Xenopus oocyte.. Acta Pharmacol Sin 2004 Jan;25(1):90-7.
            pubmed: 14704128
          32. Maggiorini M, Mélot C, Pierre S, Pfeiffer F, Greve I, Sartori C, Lepori M, Hauser M, Scherrer U, Naeije R. High-altitude pulmonary edema is initially caused by an increase in capillary pressure.. Circulation 2001 Apr 24;103(16):2078-83.
            pubmed: 11319198doi: 10.1161/01.cir.103.16.2078google scholar: lookup
          33. Maren TH. Carbonic anhydrase: chemistry, physiology, and inhibition.. Physiol Rev 1967 Oct;47(4):595-781.
            pubmed: 4964060doi: 10.1152/physrev.1967.47.4.595google scholar: lookup
          34. Marshall BE, Marshall C, Magno M, Lilagan P, Pietra GG. Influence of bronchial arterial PO2 on pulmonary vascular resistance.. J Appl Physiol (1985) 1991 Jan;70(1):405-15.
            pubmed: 2010399doi: 10.1152/jappl.1991.70.1.405google scholar: lookup
          35. McKelvie RS, Lindinger MI, Heigenhauser GJ, Jones NL. Contribution of erythrocytes to the control of the electrolyte changes of exercise.. Can J Physiol Pharmacol 1991 Jul;69(7):984-93.
            pubmed: 1954568doi: 10.1139/y91-148google scholar: lookup
          36. McKenna MJ, Heigenhauser GJ, McKelvie RS, MacDougall JD, Jones NL. Sprint training enhances ionic regulation during intense exercise in men.. J Physiol 1997 Jun 15;501 ( Pt 3)(Pt 3):687-702.
          37. McKenzie DC, O'Hare TJ, Mayo J. The effect of sustained heavy exercise on the development of pulmonary edema in trained male cyclists.. Respir Physiol Neurobiol 2005 Feb 15;145(2-3):209-18.
            pubmed: 15705536doi: 10.1016/j.resp.2004.06.010google scholar: lookup
          38. Morray JP, Lynn AM, Mansfield PB. Effect of pH and PCO2 on pulmonary and systemic hemodynamics after surgery in children with congenital heart disease and pulmonary hypertension.. J Pediatr 1988 Sep;113(3):474-9.
            pubmed: 3137318doi: 10.1016/s0022-3476(88)80631-0google scholar: lookup
          39. Newman JH, Butka BJ, Parker RE, Roselli RJ. Effect of progressive exercise on lung fluid balance in sheep.. J Appl Physiol (1985) 1988 May;64(5):2125-31.
            pubmed: 3391911doi: 10.1152/jappl.1988.64.5.2125google scholar: lookup
          40. Parker JC, Stevens T, Randall J, Weber DS, King JA. Hydraulic conductance of pulmonary microvascular and macrovascular endothelial cell monolayers.. Am J Physiol Lung Cell Mol Physiol 2006 Jul;291(1):L30-7.
            pubmed: 16760315doi: 10.1152/ajplung.00317.2005google scholar: lookup
          41. Rose RJ, Hodgson DR, Kelso TB, McCutcheon LJ, Bayly WM, Gollnick PD. Effects of acetazolamide on metabolic and respiratory responses to exercise at maximal O2 uptake.. J Appl Physiol (1985) 1990 Feb;68(2):617-26.
            pubmed: 2318772doi: 10.1152/jappl.1990.68.2.617google scholar: lookup
          42. Rudolph AM, Yuan S. Response of the pulmonary vasculature to hypoxia and H+ ion concentration changes.. J Clin Invest 1966 Mar;45(3):399-411.
            pmc: PMC292711pubmed: 5904557doi: 10.1172/jci105355google scholar: lookup
          43. Shirai M, Sada K, Ninomiya I. Effects of regional alveolar hypoxia and hypercapnia on small pulmonary vessels in cats.. J Appl Physiol (1985) 1986 Aug;61(2):440-8.
            pubmed: 3091565doi: 10.1152/jappl.1986.61.2.440google scholar: lookup
          44. Sinha AK, Gleed RD, Hakim TS, Dobson A, Shannon KJ. Pulmonary capillary pressure during exercise in horses.. J Appl Physiol (1985) 1996 May;80(5):1792-8.
            pubmed: 8727568doi: 10.1152/jappl.1996.80.5.1792google scholar: lookup
          45. Schaffartzik W, Poole DC, Derion T, Tsukimoto K, Hogan MC, Arcos JP, Bebout DE, Wagner PD. VA/Q distribution during heavy exercise and recovery in humans: implications for pulmonary edema.. J Appl Physiol (1985) 1992 May;72(5):1657-67.
            pubmed: 1601769doi: 10.1152/jappl.1992.72.5.1657google scholar: lookup
          46. Schaffartzik W, Arcos J, Tsukimoto K, Mathieu-Costello O, Wagner PD. Pulmonary interstitial edema in the pig after heavy exercise.. J Appl Physiol (1985) 1993 Dec;75(6):2535-40.
            pubmed: 8125872doi: 10.1152/jappl.1993.75.6.2535google scholar: lookup
          47. Schneeberger EE, Karnovsky MJ. Substructure of intercellular junctions in freeze-fractured alveolar-capillary membranes of mouse lung.. Circ Res 1976 May;38(5):404-11.
            pubmed: 1269080doi: 10.1161/01.res.38.5.404google scholar: lookup
          48. Shimoda LA, Luke T, Sylvester JT, Shih HW, Jain A, Swenson ER. Inhibition of hypoxia-induced calcium responses in pulmonary arterial smooth muscle by acetazolamide is independent of carbonic anhydrase inhibition.. Am J Physiol Lung Cell Mol Physiol 2007 Apr;292(4):L1002-12.
            pubmed: 17209136doi: 10.1152/ajplung.00161.2006google scholar: lookup
          49. Søgaard R, Zeuthen T. Test of blockers of AQP1 water permeability by a high-resolution method: no effects of tetraethylammonium ions or acetazolamide.. Pflugers Arch 2008 May;456(2):285-92.
            pubmed: 18043939doi: 10.1007/s00424-007-0392-2google scholar: lookup
          50. Sterling D, Reithmeier RA, Casey JR. Carbonic anhydrase: in the driver's seat for bicarbonate transport.. JOP 2001 Jul;2(4 Suppl):165-70.
            pubmed: 11875254
          51. Swenson ER, Maren TH. A quantitative analysis of CO2 transport at rest and during maximal exercise.. Respir Physiol 1978 Nov;35(2):129-59.
            pubmed: 105387doi: 10.1016/0034-5687(78)90018-xgoogle scholar: lookup
          52. Tanimura Y, Hiroaki Y, Fujiyoshi Y. Acetazolamide reversibly inhibits water conduction by aquaporin-4.. J Struct Biol 2009 Apr;166(1):16-21.
            pubmed: 19114109doi: 10.1016/j.jsb.2008.11.010google scholar: lookup
          53. Teppema LJ, Balanos GM, Steinback CD, Brown AD, Foster GE, Duff HJ, Leigh R, Poulin MJ. Effects of acetazolamide on ventilatory, cerebrovascular, and pulmonary vascular responses to hypoxia.. Am J Respir Crit Care Med 2007 Feb 1;175(3):277-81.
            pubmed: 17095745doi: 10.1164/rccm.200608-1199ocgoogle scholar: lookup
          54. van't Hoff JH. Die Rolle osmotischen Drucks in der Analogie zwischen Losungen und Gasen. Z Phys Chem 1887;1:481–508.
          55. Vengust M, Staempfli H, Viel L, Heigenhauser G. Transvascular fluid flux from the pulmonary vasculature at rest and during exercise in horses.. J Physiol 2006 Jan 15;570(Pt 2):397-405.
          56. Vengust M, Staempfli H, Viel L, Heigenhauser G. Effects of chronic acetazolamide administration on fluid flux from the pulmonary vasculature at rest and during exercise in horses.. Equine Vet J Suppl 2006 Aug;(36):508-15.
          57. Vengust M, Kerr C, Staempfli HR, Pringle J, Heigenhauser GJ, Viel L. Effect of frusemide on transvascular fluid fluxes across the lung in exercising horses.. Equine Vet J 2011 Jul;43(4):451-9.
          58. Wagner PD, Gillespie JR, Landgren GL, Fedde MR, Jones BW, DeBowes RM, Pieschl RL, Erickson HH. Mechanism of exercise-induced hypoxemia in horses.. J Appl Physiol (1985) 1989 Mar;66(3):1227-33.
            pubmed: 2496088doi: 10.1152/jappl.1989.66.3.1227google scholar: lookup
          59. West JB, Mathieu-Costello O, Jones JH, Birks EK, Logemann RB, Pascoe JR, Tyler WS. Stress failure of pulmonary capillaries in racehorses with exercise-induced pulmonary hemorrhage.. J Appl Physiol (1985) 1993 Sep;75(3):1097-109.
            pubmed: 8226517doi: 10.1152/jappl.1993.75.3.1097google scholar: lookup
          60. Wilkins PA, Gleed RD, Krivitski NM, Dobson A. Extravascular lung water in the exercising horse.. J Appl Physiol (1985) 2001 Dec;91(6):2442-50.
            pubmed: 11717203doi: 10.1152/jappl.2001.91.6.2442google scholar: lookup
          61. Yang B, Kim JK, Verkman AS. Comparative efficacy of HgCl2 with candidate aquaporin-1 inhibitors DMSO, gold, TEA+ and acetazolamide.. FEBS Lett 2006 Dec 11;580(28-29):6679-84.
          62. Younes M, Bshouty Z, Ali J. Longitudinal distribution of pulmonary vascular resistance with very high pulmonary blood flow.. J Appl Physiol (1985) 1987 Jan;62(1):344-58.
            pubmed: 3558193doi: 10.1152/jappl.1987.62.1.344google scholar: lookup

          Citations

          This article has been cited 2 times.
          1. Barpujari A, Pierre K, Dodd W, Dagra A, Small C, Williams E, Clark A, Lucke-Wold B. Lessons from NATURE: methods for traumatic brain injury prevention.. Arch Clin Toxicol (Middlet) 2021;3(1):34-41.
            pubmed: 34993525
          2. Frlic O, Seliškar A, Domanjko Petrič A, Blagus R, Heigenhauser G, Vengust M. Pulmonary Circulation Transvascular Fluid Fluxes Do Not Change during General Anesthesia in Dogs.. Front Physiol 2018;9:124.
            doi: 10.3389/fphys.2018.00124pubmed: 29515463google scholar: lookup