Impaired microcirculatory perfusion in a rat model of cardiopulmonary bypass: the role of hemodilution

Nick J. Koning, Fellery de lange, Alexander B. A. Vonk, Yunus Ahmed, Charissa E. van den Brom, Sylvia Bogaards, Matijs van Meurs, Rianne M. Jongman, Casper G. Schalkwijk, Mark P. V. Begieneman, Hans W. Niessen, Christophe Baufreton, Christa Boer

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Although hemodilution is attributed as the main cause of microcirculatory impairment during cardiopulmonary bypass (CPB), this relationship has never been investigated. We investigated the distinct effects of hemodilution with or without CPB on microvascular perfusion and subsequent renal tissue injury in a rat model. Male Wistar rats (375-425 g) were anesthetized, prepared for cremaster muscle intravital microscopy, and subjected to CPB (n = 9), hemodilution alone (n = 9), or a sham procedure (n = 6). Microcirculatory recordings were performed at multiple time points and analyzed for perfusion characteristics. Kidney and lung tissue were investigated for mRNA expression for genes regulating inflammation and endothelial adhesion molecule expression. Renal injury was assessed with immunohistochemistry. Hematocrit levels dropped to 0.24 ± 0.03 l/l and 0.22 ± 0.02 l/l after onset of hemodilution with or without CPB. Microcirculatory perfusion remained unaltered in sham rats. Hemodilution alone induced a 13% decrease in perfused capillaries, after which recovery was observed. Onset of CPB reduced the perfused capillaries by 40% (9.2 ± 0.9 to 5.5 ± 1.5 perfused capillaries per microscope field; P < 0.001), and this reduction persisted throughout the experiment. Endothelial and inflammatory activation and renal histological injury were increased after CPB compared with hemodilution or sham procedure. Hemodilution leads to minor and transient disturbances in microcirculatory perfusion, which cannot fully explain impaired microcirculation following cardiopulmonary bypass. CPB led to increased renal injury and endothelial adhesion molecule expression in the kidney and lung compared with hemodilution. Our findings suggest that microcirculatory impairment during CPB may play a role in the development of kidney injury.

Original languageEnglish
Pages (from-to)H550-H558
JournalAmerican Journal of Physiology. Heart and Circulatory Physiology
Volume310
Issue number5
DOIs
Publication statusPublished - 1 Mar 2016

Cite this

Koning, Nick J. ; de lange, Fellery ; Vonk, Alexander B. A. ; Ahmed, Yunus ; van den Brom, Charissa E. ; Bogaards, Sylvia ; van Meurs, Matijs ; Jongman, Rianne M. ; Schalkwijk, Casper G. ; Begieneman, Mark P. V. ; Niessen, Hans W. ; Baufreton, Christophe ; Boer, Christa. / Impaired microcirculatory perfusion in a rat model of cardiopulmonary bypass : the role of hemodilution. In: American Journal of Physiology. Heart and Circulatory Physiology. 2016 ; Vol. 310, No. 5. pp. H550-H558.
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abstract = "Although hemodilution is attributed as the main cause of microcirculatory impairment during cardiopulmonary bypass (CPB), this relationship has never been investigated. We investigated the distinct effects of hemodilution with or without CPB on microvascular perfusion and subsequent renal tissue injury in a rat model. Male Wistar rats (375-425 g) were anesthetized, prepared for cremaster muscle intravital microscopy, and subjected to CPB (n = 9), hemodilution alone (n = 9), or a sham procedure (n = 6). Microcirculatory recordings were performed at multiple time points and analyzed for perfusion characteristics. Kidney and lung tissue were investigated for mRNA expression for genes regulating inflammation and endothelial adhesion molecule expression. Renal injury was assessed with immunohistochemistry. Hematocrit levels dropped to 0.24 ± 0.03 l/l and 0.22 ± 0.02 l/l after onset of hemodilution with or without CPB. Microcirculatory perfusion remained unaltered in sham rats. Hemodilution alone induced a 13{\%} decrease in perfused capillaries, after which recovery was observed. Onset of CPB reduced the perfused capillaries by 40{\%} (9.2 ± 0.9 to 5.5 ± 1.5 perfused capillaries per microscope field; P < 0.001), and this reduction persisted throughout the experiment. Endothelial and inflammatory activation and renal histological injury were increased after CPB compared with hemodilution or sham procedure. Hemodilution leads to minor and transient disturbances in microcirculatory perfusion, which cannot fully explain impaired microcirculation following cardiopulmonary bypass. CPB led to increased renal injury and endothelial adhesion molecule expression in the kidney and lung compared with hemodilution. Our findings suggest that microcirculatory impairment during CPB may play a role in the development of kidney injury.",
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author = "Koning, {Nick J.} and {de lange}, Fellery and Vonk, {Alexander B. A.} and Yunus Ahmed and {van den Brom}, {Charissa E.} and Sylvia Bogaards and {van Meurs}, Matijs and Jongman, {Rianne M.} and Schalkwijk, {Casper G.} and Begieneman, {Mark P. V.} and Niessen, {Hans W.} and Christophe Baufreton and Christa Boer",
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Impaired microcirculatory perfusion in a rat model of cardiopulmonary bypass : the role of hemodilution. / Koning, Nick J.; de lange, Fellery; Vonk, Alexander B. A.; Ahmed, Yunus; van den Brom, Charissa E.; Bogaards, Sylvia; van Meurs, Matijs; Jongman, Rianne M.; Schalkwijk, Casper G.; Begieneman, Mark P. V.; Niessen, Hans W.; Baufreton, Christophe; Boer, Christa.

In: American Journal of Physiology. Heart and Circulatory Physiology, Vol. 310, No. 5, 01.03.2016, p. H550-H558.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Impaired microcirculatory perfusion in a rat model of cardiopulmonary bypass

T2 - the role of hemodilution

AU - Koning, Nick J.

AU - de lange, Fellery

AU - Vonk, Alexander B. A.

AU - Ahmed, Yunus

AU - van den Brom, Charissa E.

AU - Bogaards, Sylvia

AU - van Meurs, Matijs

AU - Jongman, Rianne M.

AU - Schalkwijk, Casper G.

AU - Begieneman, Mark P. V.

AU - Niessen, Hans W.

AU - Baufreton, Christophe

AU - Boer, Christa

N1 - Copyright © 2016 the American Physiological Society.

PY - 2016/3/1

Y1 - 2016/3/1

N2 - Although hemodilution is attributed as the main cause of microcirculatory impairment during cardiopulmonary bypass (CPB), this relationship has never been investigated. We investigated the distinct effects of hemodilution with or without CPB on microvascular perfusion and subsequent renal tissue injury in a rat model. Male Wistar rats (375-425 g) were anesthetized, prepared for cremaster muscle intravital microscopy, and subjected to CPB (n = 9), hemodilution alone (n = 9), or a sham procedure (n = 6). Microcirculatory recordings were performed at multiple time points and analyzed for perfusion characteristics. Kidney and lung tissue were investigated for mRNA expression for genes regulating inflammation and endothelial adhesion molecule expression. Renal injury was assessed with immunohistochemistry. Hematocrit levels dropped to 0.24 ± 0.03 l/l and 0.22 ± 0.02 l/l after onset of hemodilution with or without CPB. Microcirculatory perfusion remained unaltered in sham rats. Hemodilution alone induced a 13% decrease in perfused capillaries, after which recovery was observed. Onset of CPB reduced the perfused capillaries by 40% (9.2 ± 0.9 to 5.5 ± 1.5 perfused capillaries per microscope field; P < 0.001), and this reduction persisted throughout the experiment. Endothelial and inflammatory activation and renal histological injury were increased after CPB compared with hemodilution or sham procedure. Hemodilution leads to minor and transient disturbances in microcirculatory perfusion, which cannot fully explain impaired microcirculation following cardiopulmonary bypass. CPB led to increased renal injury and endothelial adhesion molecule expression in the kidney and lung compared with hemodilution. Our findings suggest that microcirculatory impairment during CPB may play a role in the development of kidney injury.

AB - Although hemodilution is attributed as the main cause of microcirculatory impairment during cardiopulmonary bypass (CPB), this relationship has never been investigated. We investigated the distinct effects of hemodilution with or without CPB on microvascular perfusion and subsequent renal tissue injury in a rat model. Male Wistar rats (375-425 g) were anesthetized, prepared for cremaster muscle intravital microscopy, and subjected to CPB (n = 9), hemodilution alone (n = 9), or a sham procedure (n = 6). Microcirculatory recordings were performed at multiple time points and analyzed for perfusion characteristics. Kidney and lung tissue were investigated for mRNA expression for genes regulating inflammation and endothelial adhesion molecule expression. Renal injury was assessed with immunohistochemistry. Hematocrit levels dropped to 0.24 ± 0.03 l/l and 0.22 ± 0.02 l/l after onset of hemodilution with or without CPB. Microcirculatory perfusion remained unaltered in sham rats. Hemodilution alone induced a 13% decrease in perfused capillaries, after which recovery was observed. Onset of CPB reduced the perfused capillaries by 40% (9.2 ± 0.9 to 5.5 ± 1.5 perfused capillaries per microscope field; P < 0.001), and this reduction persisted throughout the experiment. Endothelial and inflammatory activation and renal histological injury were increased after CPB compared with hemodilution or sham procedure. Hemodilution leads to minor and transient disturbances in microcirculatory perfusion, which cannot fully explain impaired microcirculation following cardiopulmonary bypass. CPB led to increased renal injury and endothelial adhesion molecule expression in the kidney and lung compared with hemodilution. Our findings suggest that microcirculatory impairment during CPB may play a role in the development of kidney injury.

KW - Acute Kidney Injury

KW - Acute Lung Injury

KW - Animals

KW - Capillaries

KW - Cardiopulmonary Bypass

KW - Cell Adhesion Molecules

KW - Cytokines

KW - Endothelial Cells

KW - Gene Expression Regulation

KW - Hemodilution

KW - Inflammation Mediators

KW - Intravital Microscopy

KW - Kidney

KW - Lung

KW - Male

KW - Microcirculation

KW - Models, Animal

KW - Rats, Wistar

KW - Time Factors

KW - Journal Article

KW - Research Support, Non-U.S. Gov't

U2 - 10.1152/ajpheart.00913.2015

DO - 10.1152/ajpheart.00913.2015

M3 - Article

VL - 310

SP - H550-H558

JO - American Journal of Physiology. Heart and Circulatory Physiology

JF - American Journal of Physiology. Heart and Circulatory Physiology

SN - 0363-6135

IS - 5

ER -