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Circulation Research. 1996;79:424-434

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(Circulation Research. 1996;79:424-434.)
© 1996 American Heart Association, Inc.


Articles

Time Course of Late Preconditioning Against Myocardial Stunning in Conscious Pigs

Xian-Liang Tang, Yumin Qiu, Seong-Wook Park, Jian-Zhong Sun, Anantharam Kalya, Roberto Bolli

the Experimental Research Laboratory, Section of Cardiology, Department of Medicine, Baylor College of Medicine (X.-L.T., Y.Q., S.-W.P., J.-Z.S., R.B.), Houston, Tex, and the Experimental Research Laboratory, Division of Cardiology, University of Louisville (X.-L.T., Y.Q., A.K., R.B.), Louisville, Ky.

Correspondence to Roberto Bolli, MD, Division of Cardiology, University of Louisville, Louisville, KY 40292. E-mail r0boll01@ulkyvm.louisville.edu.

We have recently found in conscious pigs that a sequence of brief coronary occlusions induces severe myocardial stunning, but when the same sequence is repeated 24 hours later, the severity of stunning is markedly reduced ({approx}50%) ("late preconditioning against stunning"). As an initial step toward elucidating the mechanism and potential clinical significance of this powerful cardioprotective response, the present study was conducted to define the time course of late preconditioning against myocardial stunning. Conscious pigs underwent a sequence of ten 2-minute coronary occlusion/2-minute reperfusion cycles and then a second identical sequence at 6 hours (group I, n=7), 12 hours (group II, n=6), 24 hours (group III, n=10), 3 days (group IV, n=10), or 6 days (group V, n=11) after the first. Systolic wall thickening (WTh) in the ischemic/reperfused region remained significantly depressed for at least 3 hours after the 10th reperfusion of the first sequence, indicating myocardial stunning. When the second sequence of coronary occlusions was performed 6 hours after the first (group I), the recovery of WTh was similar to the first. In contrast, when the second sequence was repeated 12 hours after the first (group II), the recovery of WTh was improved, though not consistently, and the total deficit of WTh decreased by 41% (P<.05) compared with the first sequence. When the second sequence was repeated 24 hours (group III) and 3 days (group IV) after the first, the recovery of WTh was substantially enhanced, with 52% and 49% reductions in the total deficit of WTh, respectively (P<.01 versus the first sequence). When the second sequence was repeated 6 days later (group V), the recovery of WTh was indistinguishable from the first sequence. Thus, late preconditioning against myocardial stunning requires >6 hours to develop, lasts for at least 60 hours after its appearance (with the most effective protection present at 24 hours and 3 days), and disappears within 6 days after the preconditioning ischemia, a time course that is consistent with the synthesis and degradation of cardioprotective proteins. In view of its sustained duration, this endogenous cardioprotective mechanism is of potential clinical importance.


Key Words: ischemic preconditioning • myocardial stunning • contractile function • thickening fraction • pig




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[Abstract] [Full Text] [PDF]


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[Abstract] [Full Text] [PDF]


Home page
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Circ. Res., July 27, 1998; 83(2): 117 - 132.
[Abstract] [Full Text] [PDF]


Home page
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Cardiovasc Res, June 1, 1998; 38(3): 549 - 558.
[Full Text] [PDF]


Home page
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Cardiovasc Res, January 1, 1998; 37(1): 21 - 33.
[Abstract] [Full Text] [PDF]


Home page
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Circ. Res., December 19, 1997; 81(6): 1094 - 1107.
[Abstract] [Full Text]


Home page
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Home page
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Am J Physiol Heart Circ Physiol, October 1, 1997; 273(4): H1651 - H1657.
[Abstract] [Full Text] [PDF]


Home page
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Home page
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Cardiovasc Res, August 1, 1997; 35(2): 233 - 240.
[Abstract] [Full Text] [PDF]


Home page
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Circ. Res., July 19, 1997; 81(1): 42 - 52.
[Abstract] [Full Text]


Home page
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Circ. Res., May 19, 1997; 80(5): 730 - 742.
[Abstract] [Full Text]


Home page
Circ. Res.Home page
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Role of Protein Kinase C in Ischemic Preconditioning: Player or Spectator?
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