Skip to main content
Top
Published in: BMC Surgery 1/2011

Open Access 01-12-2011 | Research article

Acute effects of remote ischemic preconditioning on cutaneous microcirculation - a controlled prospective cohort study

Authors: Robert Kraemer, Johan Lorenzen, Mohammad Kabbani, Christian Herold, Marc Busche, Peter M Vogt, Karsten Knobloch

Published in: BMC Surgery | Issue 1/2011

Login to get access

Abstract

Background

Therapeutic strategies aiming to reduce ischemia/reperfusion injury by conditioning tissue tolerance against ischemia appear attractive not only from a scientific perspective, but also in clinics. Although previous studies indicate that remote ischemic intermittent preconditioning (RIPC) is a systemic phenomenon, only a few studies have focused on the elucidation of its mechanisms of action especially in the clinical setting. Therefore, the aim of this study is to evaluate the acute microcirculatory effects of remote ischemic preconditioning on a distinct cutaneous location at the lower extremity which is typically used as a harvesting site for free flap reconstructive surgery in a human in-vivo setting.

Methods

Microcirculatory data of 27 healthy subjects (25 males, age 24 ± 4 years, BMI 23.3) were evaluated continuously at the anterolateral aspect of the left thigh during RIPC using combined Laser-Doppler and photospectrometry (Oxygen-to-see, Lea Medizintechnik, Germany). After baseline microcirculatory measurement, remote ischemia was induced using a tourniquet on the contralateral upper arm for three cycles of 5 min.

Results

After RIPC, tissue oxygen saturation and capillary blood flow increased up to 29% and 35% during the third reperfusion phase versus baseline measurement, respectively (both p = 0.001). Postcapillary venous filling pressure decreased statistically significant by 16% during second reperfusion phase (p = 0.028).

Conclusion

Remote intermittent ischemic preconditioning affects cutaneous tissue oxygen saturation, arterial capillary blood flow and postcapillary venous filling pressure at a remote cutaneous location of the lower extremity. To what extent remote preconditioning might ameliorate reperfusion injury in soft tissue trauma or free flap transplantation further clinical trials have to evaluate.

Trial registration

ClinicalTrials.gov: NCT01235286
Appendix
Available only for authorised users
Literature
1.
go back to reference Lorenzo AR, Lin CH, Lin CH, Lin YT, Nguyen A, Hsu CC, Wei FC: Selection of the recipient vein in microvascular flap reconstruction of the lower extremity: Analysis of 362 free-tissue transfers. J Plast Reconstr Aesthet Surg. 2011, 64 (5): 649-55. 10.1016/j.bjps.2010.07.028. Epub 2010 Aug 21CrossRefPubMed Lorenzo AR, Lin CH, Lin CH, Lin YT, Nguyen A, Hsu CC, Wei FC: Selection of the recipient vein in microvascular flap reconstruction of the lower extremity: Analysis of 362 free-tissue transfers. J Plast Reconstr Aesthet Surg. 2011, 64 (5): 649-55. 10.1016/j.bjps.2010.07.028. Epub 2010 Aug 21CrossRefPubMed
2.
go back to reference Nahabedian MY, Momen B, Manson PN: Factors associated with anastomotic failure after microvascular reconstruction of the breast. Plast Reconstr Surg. 2004, 114: 74e82- Nahabedian MY, Momen B, Manson PN: Factors associated with anastomotic failure after microvascular reconstruction of the breast. Plast Reconstr Surg. 2004, 114: 74e82-
3.
go back to reference Moran SL, Serletti JM: Outcome comparison between free and pedicled TRAM flap breast reconstruction in the obesepatient. Plast Reconstr Surg. 2001, 108: 1954e60-[discussion:61e2]CrossRef Moran SL, Serletti JM: Outcome comparison between free and pedicled TRAM flap breast reconstruction in the obesepatient. Plast Reconstr Surg. 2001, 108: 1954e60-[discussion:61e2]CrossRef
4.
go back to reference Cleveland JC, Meldrum DR, Rowland RT, Banerjee A, Harken AH: Preconditioning and hypothermic cardioplegia protect human heart equally against ischemia. Ann Thorac Surg. 1997, 63: 147e52-CrossRef Cleveland JC, Meldrum DR, Rowland RT, Banerjee A, Harken AH: Preconditioning and hypothermic cardioplegia protect human heart equally against ischemia. Ann Thorac Surg. 1997, 63: 147e52-CrossRef
5.
go back to reference Friehs I, Moran AM, Stamm C, Choi YH, Cowan DB, McGowan FX, del Nido PJ: Promoting angiogenesis protects severely hypertrophied hearts from ischemic injury. Ann Thorac Surg. 2004, 77: 2004e10-[discussion: 11] Friehs I, Moran AM, Stamm C, Choi YH, Cowan DB, McGowan FX, del Nido PJ: Promoting angiogenesis protects severely hypertrophied hearts from ischemic injury. Ann Thorac Surg. 2004, 77: 2004e10-[discussion: 11]
6.
go back to reference Koti RS, Seifalian AM, McBride AG, Yang W, Davidson BR: The relationship of hepatic tissue oxygenation with nitric oxide metabolism in ischemic preconditioning of the liver. FASEB J. 2002, 16: 1654-1656.PubMed Koti RS, Seifalian AM, McBride AG, Yang W, Davidson BR: The relationship of hepatic tissue oxygenation with nitric oxide metabolism in ischemic preconditioning of the liver. FASEB J. 2002, 16: 1654-1656.PubMed
7.
go back to reference Kharbanda RK, Mortensen UM, White PA, Kristiansen SB, Schmidt MR, Hoschtitzky JA, Vogel M, Sorensen K, Redington AN, MacAllister R: Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation. 2002, 106: 2881-10.1161/01.CIR.0000043806.51912.9B.CrossRefPubMed Kharbanda RK, Mortensen UM, White PA, Kristiansen SB, Schmidt MR, Hoschtitzky JA, Vogel M, Sorensen K, Redington AN, MacAllister R: Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation. 2002, 106: 2881-10.1161/01.CIR.0000043806.51912.9B.CrossRefPubMed
8.
go back to reference Mounsey RA, Pang CY, Boyd JB, Forrest C: Augmentation of skeletal muscle survival in the latissimus dorsi porcine model using acute ischemic preconditioning. J Otolaryngol. 1992, 21: 315e20- Mounsey RA, Pang CY, Boyd JB, Forrest C: Augmentation of skeletal muscle survival in the latissimus dorsi porcine model using acute ischemic preconditioning. J Otolaryngol. 1992, 21: 315e20-
9.
go back to reference Adanali G, Ozer K, Siemionow M: Early and late effects of ischemic preconditioning on microcirculation of skeletal muscle flaps. Plast Reconstr Surg. 2002, 109: 1344e51-CrossRef Adanali G, Ozer K, Siemionow M: Early and late effects of ischemic preconditioning on microcirculation of skeletal muscle flaps. Plast Reconstr Surg. 2002, 109: 1344e51-CrossRef
10.
go back to reference Zhang F, Oswald T, Holt J, Gerzenshtein J, Lei MP, Lineaweaver WC: Regulation of inducible nitric oxide synthase in ischemic preconditioning of muscle flap in a rat model. Ann Plast Surg. 2004, 52: 609e13-CrossRef Zhang F, Oswald T, Holt J, Gerzenshtein J, Lei MP, Lineaweaver WC: Regulation of inducible nitric oxide synthase in ischemic preconditioning of muscle flap in a rat model. Ann Plast Surg. 2004, 52: 609e13-CrossRef
11.
go back to reference Kinnunen I, Laurikainen E, Schrey A, Laippala P, Aitasalo K: Effect of acute ischemic preconditioning on blood-flow response in the epigastric pedicled rat flap. J Reconstr Microsurg. 2002, 18: 61e8- Kinnunen I, Laurikainen E, Schrey A, Laippala P, Aitasalo K: Effect of acute ischemic preconditioning on blood-flow response in the epigastric pedicled rat flap. J Reconstr Microsurg. 2002, 18: 61e8-
12.
go back to reference Scheufler O, Andresen R, Kirsch A, Banzer D, Vaubel E: Clinical results of TRAM flap delay by selective embolization of the deep inferior epigastric arteries. Plast Reconstr Surg. 2000, 105: 1320e9- Scheufler O, Andresen R, Kirsch A, Banzer D, Vaubel E: Clinical results of TRAM flap delay by selective embolization of the deep inferior epigastric arteries. Plast Reconstr Surg. 2000, 105: 1320e9-
13.
go back to reference Vandenbroucke JP, von Elm E, Altman DG, Gøtzsche PC, Mulrow CD, Pocock SJ, Poole C, Schlesselman JJ, Egger M, STROBE initiative: Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. Ann Intern Med. 2007, 147 (8): W163-94.CrossRefPubMed Vandenbroucke JP, von Elm E, Altman DG, Gøtzsche PC, Mulrow CD, Pocock SJ, Poole C, Schlesselman JJ, Egger M, STROBE initiative: Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. Ann Intern Med. 2007, 147 (8): W163-94.CrossRefPubMed
14.
go back to reference Frank KH, Kessler M, Appelaum K, Dümmler W: The erlangen micro-lightguide spectrophotometer EMPHO I. Phys Med Biol. 1989, 34: 1883-1900. 10.1088/0031-9155/34/12/011.CrossRefPubMed Frank KH, Kessler M, Appelaum K, Dümmler W: The erlangen micro-lightguide spectrophotometer EMPHO I. Phys Med Biol. 1989, 34: 1883-1900. 10.1088/0031-9155/34/12/011.CrossRefPubMed
15.
go back to reference Menger MD, Pelikan S, Steiner D, Messmer K: Microvascular ischemia-reperfusion injury in striated muscle: significance of ''reflow paradox''. Am J Physiol. 1992, 263: H1901e6- Menger MD, Pelikan S, Steiner D, Messmer K: Microvascular ischemia-reperfusion injury in striated muscle: significance of ''reflow paradox''. Am J Physiol. 1992, 263: H1901e6-
16.
go back to reference Pang CY, Yang RZ, Zhong A, Xu N, Boyd B, Forrest CR: Acute ischaemic preconditioning protects against skeletal muscle infarction in the pig. Cardiovasc Res. 1995, 29: 782e8-CrossRef Pang CY, Yang RZ, Zhong A, Xu N, Boyd B, Forrest CR: Acute ischaemic preconditioning protects against skeletal muscle infarction in the pig. Cardiovasc Res. 1995, 29: 782e8-CrossRef
17.
go back to reference Wang WZ, Anderson G, Maldonado C, Barker J: Attenuation of vasospasm and capillary no-reflow by ischemic preconditioning in skeletal muscle. Microsurgery. 1996, 17: 324e9-CrossRef Wang WZ, Anderson G, Maldonado C, Barker J: Attenuation of vasospasm and capillary no-reflow by ischemic preconditioning in skeletal muscle. Microsurgery. 1996, 17: 324e9-CrossRef
18.
go back to reference Wang WZ, Anderson G, Firrell JC, Tsai TM: Ischemic preconditioning versus intermittent reperfusion to improve blood flow to a vascular isolated skeletal muscle flap of rats. J Trauma. 1998, 45: 953e9-CrossRef Wang WZ, Anderson G, Firrell JC, Tsai TM: Ischemic preconditioning versus intermittent reperfusion to improve blood flow to a vascular isolated skeletal muscle flap of rats. J Trauma. 1998, 45: 953e9-CrossRef
19.
go back to reference Adanali G, Ozer K, Siemionow M: Early and late effects of ischemic preconditioning on microcirculation of skeletal muscle flaps. Plast Reconstr Surg. 2002, 109: 1344e51-CrossRef Adanali G, Ozer K, Siemionow M: Early and late effects of ischemic preconditioning on microcirculation of skeletal muscle flaps. Plast Reconstr Surg. 2002, 109: 1344e51-CrossRef
20.
go back to reference Küntscher MV, Schirmbeck EU, Menke H, Klar E, Gebhard MM, Germann G: Ischemic preconditioning by brief extremity ischemia before flap ischemia in a rat model. Plast Reconstr Surg. 2002, 109: 2398e404- Küntscher MV, Schirmbeck EU, Menke H, Klar E, Gebhard MM, Germann G: Ischemic preconditioning by brief extremity ischemia before flap ischemia in a rat model. Plast Reconstr Surg. 2002, 109: 2398e404-
21.
go back to reference Tapuria N, Junnarkar SP, Dutt N, Abu-Amara M, Fuller B, Seifalian AM, Davidson BR: Effect of remote ischemic preconditioning on hepatic microcirculation and function in a rat model of hepatic ischemia reperfusion injury. HPB (Oxford). 2009, 11 (2): 108-17.CrossRef Tapuria N, Junnarkar SP, Dutt N, Abu-Amara M, Fuller B, Seifalian AM, Davidson BR: Effect of remote ischemic preconditioning on hepatic microcirculation and function in a rat model of hepatic ischemia reperfusion injury. HPB (Oxford). 2009, 11 (2): 108-17.CrossRef
22.
go back to reference Hoole SP, Heck PM, White PA, Khan SN, O'Sullivan M, Clarke SC, Dutka DP: Remote ischemic preconditioning stimulus does not reduce microvascular resistance or improve myocardial blood flow in patients undergoing elective percutaneous coronary intervention. Angiology. 2009, 60 (4): 403-11. 10.1177/0003319708328921. Epub 2008 Dec 23CrossRefPubMed Hoole SP, Heck PM, White PA, Khan SN, O'Sullivan M, Clarke SC, Dutka DP: Remote ischemic preconditioning stimulus does not reduce microvascular resistance or improve myocardial blood flow in patients undergoing elective percutaneous coronary intervention. Angiology. 2009, 60 (4): 403-11. 10.1177/0003319708328921. Epub 2008 Dec 23CrossRefPubMed
23.
go back to reference Thielmann M, Kottenberg E, Boengler K, Raffelsieper C, Neuhaeuser M, Peters J, Jakob H, Heusch G: Remote ischemic preconditioning reduces myocardial injury after coronary artery bypass grafting with crystalloid cardioplegic arrest. Basic Res Cardiol. 2005, 105: 657-664.CrossRef Thielmann M, Kottenberg E, Boengler K, Raffelsieper C, Neuhaeuser M, Peters J, Jakob H, Heusch G: Remote ischemic preconditioning reduces myocardial injury after coronary artery bypass grafting with crystalloid cardioplegic arrest. Basic Res Cardiol. 2005, 105: 657-664.CrossRef
24.
go back to reference Zimmerman RF, Ezeanuna PU, Kane JC, Cleland CD, Kempananjappa TJ, Lucas FL, Kramer R: Ischemic preconditioning at a remote site prevents acute kidney injury in patients following cardiac surgery. Kidney Int. 2011, 80 (8): 861-7. 10.1038/ki.2011.156. Epub 2011 Jun 15CrossRefPubMed Zimmerman RF, Ezeanuna PU, Kane JC, Cleland CD, Kempananjappa TJ, Lucas FL, Kramer R: Ischemic preconditioning at a remote site prevents acute kidney injury in patients following cardiac surgery. Kidney Int. 2011, 80 (8): 861-7. 10.1038/ki.2011.156. Epub 2011 Jun 15CrossRefPubMed
25.
go back to reference Pedersen KR, Ravn HB, Povlsen JV, Schmidt MR, Erlandsen EJ, Hjortdal VE: Failure of remote ischemic preconditioning to reduce the risk of postoperative acute kidney injury in children undergoing operation for complex congenital heart disease: A randomized single-center study. J Thorac Cardiovasc Surg. 2011, Pedersen KR, Ravn HB, Povlsen JV, Schmidt MR, Erlandsen EJ, Hjortdal VE: Failure of remote ischemic preconditioning to reduce the risk of postoperative acute kidney injury in children undergoing operation for complex congenital heart disease: A randomized single-center study. J Thorac Cardiovasc Surg. 2011,
26.
go back to reference Peters J: Remote ischaemic preconditioning of the heart: remote questions, remote importance, or remote preconditions?. Basic Res Cardiol. 2011, 106 (4): 507-9. 10.1007/s00395-011-0187-7. Epub 2011 May 5CrossRefPubMed Peters J: Remote ischaemic preconditioning of the heart: remote questions, remote importance, or remote preconditions?. Basic Res Cardiol. 2011, 106 (4): 507-9. 10.1007/s00395-011-0187-7. Epub 2011 May 5CrossRefPubMed
27.
go back to reference Zahir KS, Syed SA, Zink JR, Restifo RJ, Thomson JG: Comparison of the effects of ischemic preconditioning and surgical delay on pedicled musculocutaneous flap survival in a rat model. Ann Plast Surg. 1998, 40: 422e8-[discussion: 8e9] Zahir KS, Syed SA, Zink JR, Restifo RJ, Thomson JG: Comparison of the effects of ischemic preconditioning and surgical delay on pedicled musculocutaneous flap survival in a rat model. Ann Plast Surg. 1998, 40: 422e8-[discussion: 8e9]
28.
go back to reference Zhang L, Bail H, Mittlmeier T, Haas NP, Schaser K: Immediate microcirculatory derangements in skeletal muscle and periosteum after closed tibial fracture. J Trauma. 2003, 54 (5): 979-85. 10.1097/01.TA.0000025796.74054.5B.CrossRefPubMed Zhang L, Bail H, Mittlmeier T, Haas NP, Schaser K: Immediate microcirculatory derangements in skeletal muscle and periosteum after closed tibial fracture. J Trauma. 2003, 54 (5): 979-85. 10.1097/01.TA.0000025796.74054.5B.CrossRefPubMed
Metadata
Title
Acute effects of remote ischemic preconditioning on cutaneous microcirculation - a controlled prospective cohort study
Authors
Robert Kraemer
Johan Lorenzen
Mohammad Kabbani
Christian Herold
Marc Busche
Peter M Vogt
Karsten Knobloch
Publication date
01-12-2011
Publisher
BioMed Central
Published in
BMC Surgery / Issue 1/2011
Electronic ISSN: 1471-2482
DOI
https://doi.org/10.1186/1471-2482-11-32

Other articles of this Issue 1/2011

BMC Surgery 1/2011 Go to the issue