The impact of selective visceral perfusion on intestinal macrohemodynamics and microhemodynamics in a porcine model of thoracic aortic cross-clamping.

J. Kalder, P. Keschenau, S.J.P. Hanssen, A. Greiner, I.C. Vermeulen Windsant, L.N. Kennes, R. Tolba, F.W. Prinzen, W.A. Buurman, M.J.H.M. Jacobs, T.A. Koeppel

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Abstract

INTRODUCTION: Despite its presumed effectiveness and clinical use, the physiology of selective visceral perfusion combined with distal aortic perfusion during open thoracoabdominal aortic surgery has not been characterized. Thus, the aim of this study was to establish a translatable model of thoracic aortic-clamping to assess the effect of selective visceral perfusion with added distal aortic perfusion on local intestinal macrohemodynamics and microhemodynamics, intestinal histopathology, and markers of inflammation and intestinal damage. METHODS: A thoracolaparotomy was performed in 15 pigs, and the aorta was exposed, including the origins of celiac trunk and superior mesenteric artery. The animals were divided into three cohorts: control (I), thoracic aortic cross-clamping (II), and thoracic aortic cross-clamping with selective visceral perfusion plus distal aortic perfusion using extracorporeal circulation (III). Macrocirculatory and microcirculatory blood flow was assessed by transit time ultrasound volume flow measurements and fluorescent microspheres. Intestinal ischemia-reperfusion injury was determined by the analysis of perioperative intestinal fatty acid-binding protein (IFABP) and interleukin-8 (IL-8) levels and correlated with histopathologic changes. RESULTS: Severe intestinal tissue injury and an inflammatory response were observed in cohort II compared with cohort III for IL-8 (38.2 vs 3.56 pg/mL; P = .04). The procedure in cohort III resulted in a flow and pressure-associated intestinal hypoperfusion compared with cohort I in the superior mesenteric artery (mean blood pressure, 24.1 +/- 10.4 vs 67.2 +/- 7.4 mm Hg; P < .0001; mean flow rates: 353.3 +/- 133.8 vs 961.7 +/- 310.8 mL/min; P < .0001). This was paralleled in cohort III vs cohort I by a significant mucosal injury (IFABP, 713 +/- 307.1 vs 170 +/- 115.4 pg/mL; P = .014) despite a profound recruitment of intestinal microcirculation (338% +/- 206.7% vs 135% +/- 123.7%; P = .05). CONCLUSIONS: This study reports a novel large-animal model of thoracic aortic cross-clamping that allows the study of visceral perfusion strategies. However, we demonstrated with IL-8 and IFABP measurements that thoracoabdominal aortic aneurysm surgery with selective visceral perfusion and distal aortic perfusion is superior to the clamp-and-sew technique, even though small intestinal tissue damage cannot be completely avoided by selective visceral perfusion and distal aortic perfusion. In any case, this model seems to be a platform to evaluate and optimize measures for gut wall protection.
Original languageEnglish
Pages (from-to)149-158
JournalJournal of Vascular Surgery
Volume56
Issue number1
DOIs
Publication statusPublished - 1 Jan 2012

Cite this

Kalder, J., Keschenau, P., Hanssen, S. J. P., Greiner, A., Vermeulen Windsant, I. C., Kennes, L. N., ... Koeppel, T. A. (2012). The impact of selective visceral perfusion on intestinal macrohemodynamics and microhemodynamics in a porcine model of thoracic aortic cross-clamping. Journal of Vascular Surgery, 56(1), 149-158. https://doi.org/10.1016/j.jvs.2011.11.126
Kalder, J. ; Keschenau, P. ; Hanssen, S.J.P. ; Greiner, A. ; Vermeulen Windsant, I.C. ; Kennes, L.N. ; Tolba, R. ; Prinzen, F.W. ; Buurman, W.A. ; Jacobs, M.J.H.M. ; Koeppel, T.A. / The impact of selective visceral perfusion on intestinal macrohemodynamics and microhemodynamics in a porcine model of thoracic aortic cross-clamping. In: Journal of Vascular Surgery. 2012 ; Vol. 56, No. 1. pp. 149-158.
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title = "The impact of selective visceral perfusion on intestinal macrohemodynamics and microhemodynamics in a porcine model of thoracic aortic cross-clamping.",
abstract = "INTRODUCTION: Despite its presumed effectiveness and clinical use, the physiology of selective visceral perfusion combined with distal aortic perfusion during open thoracoabdominal aortic surgery has not been characterized. Thus, the aim of this study was to establish a translatable model of thoracic aortic-clamping to assess the effect of selective visceral perfusion with added distal aortic perfusion on local intestinal macrohemodynamics and microhemodynamics, intestinal histopathology, and markers of inflammation and intestinal damage. METHODS: A thoracolaparotomy was performed in 15 pigs, and the aorta was exposed, including the origins of celiac trunk and superior mesenteric artery. The animals were divided into three cohorts: control (I), thoracic aortic cross-clamping (II), and thoracic aortic cross-clamping with selective visceral perfusion plus distal aortic perfusion using extracorporeal circulation (III). Macrocirculatory and microcirculatory blood flow was assessed by transit time ultrasound volume flow measurements and fluorescent microspheres. Intestinal ischemia-reperfusion injury was determined by the analysis of perioperative intestinal fatty acid-binding protein (IFABP) and interleukin-8 (IL-8) levels and correlated with histopathologic changes. RESULTS: Severe intestinal tissue injury and an inflammatory response were observed in cohort II compared with cohort III for IL-8 (38.2 vs 3.56 pg/mL; P = .04). The procedure in cohort III resulted in a flow and pressure-associated intestinal hypoperfusion compared with cohort I in the superior mesenteric artery (mean blood pressure, 24.1 +/- 10.4 vs 67.2 +/- 7.4 mm Hg; P < .0001; mean flow rates: 353.3 +/- 133.8 vs 961.7 +/- 310.8 mL/min; P < .0001). This was paralleled in cohort III vs cohort I by a significant mucosal injury (IFABP, 713 +/- 307.1 vs 170 +/- 115.4 pg/mL; P = .014) despite a profound recruitment of intestinal microcirculation (338{\%} +/- 206.7{\%} vs 135{\%} +/- 123.7{\%}; P = .05). CONCLUSIONS: This study reports a novel large-animal model of thoracic aortic cross-clamping that allows the study of visceral perfusion strategies. However, we demonstrated with IL-8 and IFABP measurements that thoracoabdominal aortic aneurysm surgery with selective visceral perfusion and distal aortic perfusion is superior to the clamp-and-sew technique, even though small intestinal tissue damage cannot be completely avoided by selective visceral perfusion and distal aortic perfusion. In any case, this model seems to be a platform to evaluate and optimize measures for gut wall protection.",
author = "J. Kalder and P. Keschenau and S.J.P. Hanssen and A. Greiner and {Vermeulen Windsant}, I.C. and L.N. Kennes and R. Tolba and F.W. Prinzen and W.A. Buurman and M.J.H.M. Jacobs and T.A. Koeppel",
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Kalder, J, Keschenau, P, Hanssen, SJP, Greiner, A, Vermeulen Windsant, IC, Kennes, LN, Tolba, R, Prinzen, FW, Buurman, WA, Jacobs, MJHM & Koeppel, TA 2012, 'The impact of selective visceral perfusion on intestinal macrohemodynamics and microhemodynamics in a porcine model of thoracic aortic cross-clamping.', Journal of Vascular Surgery, vol. 56, no. 1, pp. 149-158. https://doi.org/10.1016/j.jvs.2011.11.126

The impact of selective visceral perfusion on intestinal macrohemodynamics and microhemodynamics in a porcine model of thoracic aortic cross-clamping. / Kalder, J.; Keschenau, P.; Hanssen, S.J.P.; Greiner, A.; Vermeulen Windsant, I.C.; Kennes, L.N.; Tolba, R.; Prinzen, F.W.; Buurman, W.A.; Jacobs, M.J.H.M.; Koeppel, T.A.

In: Journal of Vascular Surgery, Vol. 56, No. 1, 01.01.2012, p. 149-158.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - The impact of selective visceral perfusion on intestinal macrohemodynamics and microhemodynamics in a porcine model of thoracic aortic cross-clamping.

AU - Kalder, J.

AU - Keschenau, P.

AU - Hanssen, S.J.P.

AU - Greiner, A.

AU - Vermeulen Windsant, I.C.

AU - Kennes, L.N.

AU - Tolba, R.

AU - Prinzen, F.W.

AU - Buurman, W.A.

AU - Jacobs, M.J.H.M.

AU - Koeppel, T.A.

PY - 2012/1/1

Y1 - 2012/1/1

N2 - INTRODUCTION: Despite its presumed effectiveness and clinical use, the physiology of selective visceral perfusion combined with distal aortic perfusion during open thoracoabdominal aortic surgery has not been characterized. Thus, the aim of this study was to establish a translatable model of thoracic aortic-clamping to assess the effect of selective visceral perfusion with added distal aortic perfusion on local intestinal macrohemodynamics and microhemodynamics, intestinal histopathology, and markers of inflammation and intestinal damage. METHODS: A thoracolaparotomy was performed in 15 pigs, and the aorta was exposed, including the origins of celiac trunk and superior mesenteric artery. The animals were divided into three cohorts: control (I), thoracic aortic cross-clamping (II), and thoracic aortic cross-clamping with selective visceral perfusion plus distal aortic perfusion using extracorporeal circulation (III). Macrocirculatory and microcirculatory blood flow was assessed by transit time ultrasound volume flow measurements and fluorescent microspheres. Intestinal ischemia-reperfusion injury was determined by the analysis of perioperative intestinal fatty acid-binding protein (IFABP) and interleukin-8 (IL-8) levels and correlated with histopathologic changes. RESULTS: Severe intestinal tissue injury and an inflammatory response were observed in cohort II compared with cohort III for IL-8 (38.2 vs 3.56 pg/mL; P = .04). The procedure in cohort III resulted in a flow and pressure-associated intestinal hypoperfusion compared with cohort I in the superior mesenteric artery (mean blood pressure, 24.1 +/- 10.4 vs 67.2 +/- 7.4 mm Hg; P < .0001; mean flow rates: 353.3 +/- 133.8 vs 961.7 +/- 310.8 mL/min; P < .0001). This was paralleled in cohort III vs cohort I by a significant mucosal injury (IFABP, 713 +/- 307.1 vs 170 +/- 115.4 pg/mL; P = .014) despite a profound recruitment of intestinal microcirculation (338% +/- 206.7% vs 135% +/- 123.7%; P = .05). CONCLUSIONS: This study reports a novel large-animal model of thoracic aortic cross-clamping that allows the study of visceral perfusion strategies. However, we demonstrated with IL-8 and IFABP measurements that thoracoabdominal aortic aneurysm surgery with selective visceral perfusion and distal aortic perfusion is superior to the clamp-and-sew technique, even though small intestinal tissue damage cannot be completely avoided by selective visceral perfusion and distal aortic perfusion. In any case, this model seems to be a platform to evaluate and optimize measures for gut wall protection.

AB - INTRODUCTION: Despite its presumed effectiveness and clinical use, the physiology of selective visceral perfusion combined with distal aortic perfusion during open thoracoabdominal aortic surgery has not been characterized. Thus, the aim of this study was to establish a translatable model of thoracic aortic-clamping to assess the effect of selective visceral perfusion with added distal aortic perfusion on local intestinal macrohemodynamics and microhemodynamics, intestinal histopathology, and markers of inflammation and intestinal damage. METHODS: A thoracolaparotomy was performed in 15 pigs, and the aorta was exposed, including the origins of celiac trunk and superior mesenteric artery. The animals were divided into three cohorts: control (I), thoracic aortic cross-clamping (II), and thoracic aortic cross-clamping with selective visceral perfusion plus distal aortic perfusion using extracorporeal circulation (III). Macrocirculatory and microcirculatory blood flow was assessed by transit time ultrasound volume flow measurements and fluorescent microspheres. Intestinal ischemia-reperfusion injury was determined by the analysis of perioperative intestinal fatty acid-binding protein (IFABP) and interleukin-8 (IL-8) levels and correlated with histopathologic changes. RESULTS: Severe intestinal tissue injury and an inflammatory response were observed in cohort II compared with cohort III for IL-8 (38.2 vs 3.56 pg/mL; P = .04). The procedure in cohort III resulted in a flow and pressure-associated intestinal hypoperfusion compared with cohort I in the superior mesenteric artery (mean blood pressure, 24.1 +/- 10.4 vs 67.2 +/- 7.4 mm Hg; P < .0001; mean flow rates: 353.3 +/- 133.8 vs 961.7 +/- 310.8 mL/min; P < .0001). This was paralleled in cohort III vs cohort I by a significant mucosal injury (IFABP, 713 +/- 307.1 vs 170 +/- 115.4 pg/mL; P = .014) despite a profound recruitment of intestinal microcirculation (338% +/- 206.7% vs 135% +/- 123.7%; P = .05). CONCLUSIONS: This study reports a novel large-animal model of thoracic aortic cross-clamping that allows the study of visceral perfusion strategies. However, we demonstrated with IL-8 and IFABP measurements that thoracoabdominal aortic aneurysm surgery with selective visceral perfusion and distal aortic perfusion is superior to the clamp-and-sew technique, even though small intestinal tissue damage cannot be completely avoided by selective visceral perfusion and distal aortic perfusion. In any case, this model seems to be a platform to evaluate and optimize measures for gut wall protection.

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DO - 10.1016/j.jvs.2011.11.126

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JO - Journal of Vascular Surgery

JF - Journal of Vascular Surgery

SN - 0741-5214

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