Original Article
Abnormal Myocardial Phosphorus-31 Nuclear Magnetic Resonance Spectroscopy in Women with Chest Pain but Normal Coronary Angiograms
N Engl J Med 2000; 342:829-835March 23, 2000
- Abstract
Background
After hospitalization for chest pain, women are more likely than men to have normal coronary angiograms. In such women, myocardial ischemia in the absence of clinically significant coronary-artery obstruction has long been suspected. Most methods for the detection of the metabolic effects of myocardial ischemia are highly invasive. Phosphorus-31 nuclear magnetic resonance (31P-NMR) spectroscopy is a noninvasive technique that can directly measure high-energy phosphates in the myocardium and identify metabolic evidence of ischemia.
Methods
We enrolled 35 women who were hospitalized for chest pain but who had no angiographically significant coronary-artery obstructions and 12 age- and weight-matched control women with no evidence of heart disease. Myocardial high-energy phosphates were measured with 31P-NMR spectroscopy at 1.5 tesla before, during, and after isometric handgrip exercise at a level that was 30 percent of the maximal voluntary grip strength. We measured the change in the ratio of phosphocreatine to ATP during exercise.
Results
Seven (20 percent) of the 35 women with chest pain and no angiographically significant stenosis had decreases in the phosphocreatine:ATP ratio during handgrip that were more than 2 SD below the mean value in the control subjects without chest pain. There were no significant differences between the two groups with respect to hemodynamic variables at rest and during handgrip, risk factors for ischemic heart disease, findings on magnetic resonance imaging and radionuclide perfusion studies of the heart, or changes in brachial flow during the infusion of acetylcholine.
Conclusions
Our results provide direct evidence of an abnormal metabolic response to handgrip exercise in at least some women with chest pain consistent with the occurrence of myocardial ischemia but no angiographically significant coronary stenoses.
Media in This Article
Figure 1
Mean (±SD) and Individual Changes in Phosphocreatine:ATP Ratios during Handgrip Stress Testing in 35 Women with Chest Pain and Coronary-Artery Stenosis of 20 Percent or Less, 12 Age- and Weight-Matched Control Women with No Evidence of Heart Disease, and 11 Patients with Stenosis of at Least 70 Percent.Figure 2
Results of 31P-NMR Spectroscopy in Two Women with Chest Pain and Coronary-Artery Stenosis of 20 Percent or Less.Article Activity
- Article
According to data from the Coronary Artery Surgery Study, more than half of all women with chest pain who are referred for coronary angiography do not have angiographically significant coronary stenosis, as compared with only 17 percent of men.1 Data from the Duke Data Bank2 and Kaski et al.3 indicate a similarly low prevalence of angiographically significant coronary stenosis among women with a syndrome of chest pain. Although noncardiac causes can be responsible for the chest-pain syndrome, myocardial ischemia in the absence of angiographically significant coronary stenoses has long been a suspected cause.4,5
One strategy for the detection of ischemia in patients with chest pain and no angiographically significant coronary stenoses has focused on an evaluation of metabolic markers, including measurements of lactate production6 and the oxygen saturation of blood from the coronary sinus.7 Both these methods are invasive and subject to sampling errors.8 Phosphorus-31 nuclear magnetic resonance (31P-NMR) spectroscopy can be used to measure the myocardial high-energy phosphates phosphocreatine and ATP and to determine the ratio of phosphocreatine to ATP. Calculation of the ratio has been useful in identifying ischemia in animals9,10 and humans with coronary stenoses.11-16
We designed a multicenter study — the Women's Ischemia Syndrome Evaluation — to investigate new and innovative techniques for the detection of ischemic heart disease in women. A specific aim of the study was to investigate the prevalence and pathophysiology of myocardial ischemia in the absence of angiographically significant stenoses. Accordingly, we used the results of 31P-NMR spectroscopy during low-level isometric handgrip exercise as a metabolic marker for myocardial ischemia in women with chest pain and no angiographically significant stenoses.
Methods
Study Population
The population consisted of 35 women (age range, 31 to 72 years; mean [±SD], 57±10) who were admitted to the University of Alabama at Birmingham Medical Center with chest pain and no coronary luminal stenoses of more than 20 percent in any epicardial coronary artery according to an evaluation by the angiographic core laboratory at Rhode Island Hospital. These women underwent magnetic resonance studies of cardiac function, magnetic resonance perfusion imaging, and radionuclide myocardial perfusion imaging in addition to coronary angiography as part of the study protocol.17 A reference population was recruited to determine the response to stress induced by isometric handgrip exercise, as measured by the phosphocreatine:ATP ratio, among 12 healthy age- and weight-matched women (age range, 39 to 70 years; mean, 51±8) who had no evidence of heart disease on the basis of exercise stress testing and risk-factor analysis according to the National Cholesterol Education Program guidelines.18 A third group with stenosis of at least 70 percent in the left anterior descending coronary artery was also studied and consisted of four women and seven men. These patients ranged in age from 52 to 74 years (mean, 64±9). The angiograms of these patients were evaluated in a blinded fashion by the members of the Department of Cardiovascular Disease at the University of Alabama at Birmingham. All subjects provided informed consent, and their physicians approved their participation.
31P-NMR Spectroscopy
All subjects underwent 31P-NMR spectroscopy (Gyroscan ACS, Philips, Best, the Netherlands) at 1.5 tesla in the supine position. A 10-cm surface coil for transmission and receiving was placed over the precordium and secured with a Velcro strap to minimize respiratory artifacts. Heart rate and blood pressure were monitored throughout the procedure. After tuning and matching the surface coil, “scout” proton images were obtained in the transverse and sagittal orientations with use of a standard spin–echo technique (echo time, 28 msec). A volume of 160 to 200 cc, including the anterior wall and apex of the left ventricle but excluding the chest-wall muscle, was defined from the scout images. Appropriate adjustments were made to optimize the proton signal. We confirmed the position of the coil by identifying on the images a small vial containing phenylphosphonate located at the coil's center. This vial was also used to calibrate the 180-degree pulse. The localization technique used was image-selected in vivo spectroscopy (ISIS). Studies of phosphate solutions showed that the signal from within the designated area (voxel) accounted for 90 percent of the total signal, indicating excellent localization. The center frequency was set approximately 100 Hz up field from the phosphocreatine peak (midpoint in the spectral range). A cardiac-gated spectrum was obtained with the subject at rest with the use of adiabatic half-passage pulses. The adiabatic pulses ensure that excitation is uniform throughout the voxel. The spectral acquisition variables were as follows: repetition time, 3 seconds; 1024 points; sweep width, 2000 Hz; and 128 averages. The time required for a single spectrum ranged from 7.5 to 9 minutes, depending on the heart rate. Additional spectra were obtained during and after isometric handgrip exercise. In some cases, the heart was far enough from the coil (≥7 cm) that a coronal ISIS plane (3 to 3.5 cm thick) was used instead of a cubic voxel to increase the available signal-to-noise ratio. Location within the ISIS plane was based on the coil's sensitivity profile, which decreases in geometric fashion as the distance from the coil's center increases.
Under these conditions, it is probable that lung and liver tissue will be included in the voxel. However, lung tissue has no appreciable 31P-NMR signal in vivo, and the amount of blood contained within the lung tissue is corrected for during data processing. Liver has a strong 31P-NMR signal from ATP and monophosphates and diphosphates; however, liver has no phosphocreatine. Therefore, any measurable phosphocreatine signal must come from the myocardium. Although the recorded phosphocreatine:ATP ratio of the voxel will be lower because of the liver's contribution to the ATP signal, the relative change in the ratio as a result of stress testing will not be affected, since any change primarily reflects changes in myocardial phosphocreatine.
The nuclear magnetic resonance technique that we used differed from that used by either Weiss et al.15 or Yabe et al.,16 who used one-dimensional chemical shift imaging and depth-resolved spectroscopy, respectively. All three techniques use surface coils whose sensitivity is subject to the weighting of the measured signals according to their distance from the coil. This approach leads to a greater sensitivity to spectra generated from anterior myocardium than to spectra generated from posterior myocardium. Accordingly, the focal area in our study and the previous studies was the anterior wall (generally, the left anterior descending coronary artery). The use of a surface coil to transmit the radio frequency also causes a nonuniform excitation through the area of interest. The use of adiabatic pulses in our study ensured that excitation was uniform; however, it still did not allow adequate sampling of the posterior wall, because of the distance of the wall from the coil. Although we used a larger voxel than was used in the previous studies, a large portion of the volume included the ventricular chamber and tissue outside the myocardium, so the effective myocardial content was not greater than in the previous studies. With the elimination of skeletal muscle from the voxel, there was no potential auxiliary source of phosphocreatine.
Isometric Handgrip Exercise
A hand dynamometer (Smedley, Stoelting, Wood Dale, Ill.) was modified for use inside the whole-body magnet. Metal components that could affect the results were replaced with brass, and the spring was replaced with Tygon silicone tubing (Norton, Akron, Ohio). Calibration of the handgrip was linear over the ranges of grips obtained. To allow output to be monitored continuously without compromising the radio-frequency–shielded enclosure of the scanner, we mounted the handgrip at one end of an 8-ft (2.4 m) wooden beam and connected the handgrip to a slide potentiometer mounted at the opposite end. The output was monitored by computer (Biopac Systems, Santa Barbara, Calif.), with measurements obtained three times per second. Before entry into the whole-body magnet, the maximal voluntary grip strength of each subject was determined. During stress testing, handgrip output was maintained at 30 percent of the maximal voluntary grip strength. If the output dropped below 20 percent, the subject was asked to squeeze harder to achieve a level of 30 percent. If the heart rate and blood pressure did not return to resting levels approximately 10 minutes after testing, the subject was monitored for 10 additional minutes. The entire procedure took 65 to 75 minutes from the time the subject entered the magnet.
Among the 58 subjects, only 1 (2 percent) was unable to complete the exercise regimen and 2 (3 percent) reported mild chest pain during testing that disappeared after testing was completed. None of the subjects had ST-segment changes during testing.
Statistical Analysis
Studies and data processing were conducted with the researchers unaware of the heart disease status of the subjects. Data obtained during 31P-NMR spectroscopy were transferred to a computer workstation (Sparc 10, Sun Microsystems, Mountain View, Calif.) for processing with Sunspec and Fitmasters software (Philips), with peak positions known. The data were summed and fitted automatically after frequency offset and estimates of the starting phase had been entered. The fit of the summed data was used for processing individual spectra. The ratio of the areas of phosphocreatine and ATP were adjusted for both blood volume within the left ventricular cavity and differences in T1 between phosphocreatine and ATP. We calculated the standard deviation of the phosphocreatine:ATP ratio using the Cramér-Rao lower bound,19,20 which estimates the quality of the fit on the basis of the noise of the measurement. This value ranged from 10.6 to 16.4 percent of the ratio for all the measurements obtained. The phosphocreatine:ATP ratio and hemodynamic measurements obtained during exercise were compared with the average of the ratios obtained at rest.
We determined the variability in the results of spectrometry by making six consecutive measurements of the resting phosphocreatine:ATP ratio in a single setting in a 27-year-old man. The mean phosphocreatine:ATP ratio of all six measurements was 1.63±0.19, with the standard deviation of any individual measurement ranging from 10.6 to 13.3 percent. The reproducibility of the results of exercise stress testing was assessed in a single subject who was tested five times over a two-week period. The changes in the phosphocreatine:ATP ratio ranged from a decrease of 10 percent to an increase of 10 percent (mean, +0.6±11 percent). The threshold for an abnormal phosphocreatine:ATP ratio in response to stress testing was –22.6 percent, 2 SD below the mean value for the reference population; lower values were considered abnormal.
Among the women with chest pain and no coronary luminal stenoses of more than 20 percent, women with normal phosphocreatine:ATP ratios during stress testing were compared with women with abnormal responses with the use of t-tests for continuous data and Fisher's exact test for dichotomous data.
Results
The phosphocreatine:ATP ratios in the three study groups are summarized in Figure 1Figure 1
Mean (±SD) and Individual Changes in Phosphocreatine:ATP Ratios during Handgrip Stress Testing in 35 Women with Chest Pain and Coronary-Artery Stenosis of 20 Percent or Less, 12 Age- and Weight-Matched Control Women with No Evidence of Heart Disease, and 11 Patients with Stenosis of at Least 70 Percent.. In the reference population of 12 age- and weight-matched control women, the phosphocreatine:ATP ratio decreased by a mean of 2.6±10.0 percent in response to stress testing, a response that is similar to changes previously reported in other studies.15,16 Among the patients with stenosis of the left anterior descending coronary artery of at least 70 percent, the decrease in the phosphocreatine:ATP ratio was significantly greater (19.6± 10.7 percent, P=0.001).The response among the 35 women with chest pain and coronary-artery stenosis of no more than 20 percent spanned the range of results. Seven women in this group (20 percent) had an abnormal response during stress testing; the average decrease in the phosphocreatine:ATP ratio was 28.7±5.1 percent. Two other women had decreases that were just above the threshold. Figure 2Figure 2
Results of 31P-NMR Spectroscopy in Two Women with Chest Pain and Coronary-Artery Stenosis of 20 Percent or Less. shows the results of 31P-NMR spectroscopy for 2 of the 35 women in this group. The woman whose results are shown in Figure 2A had a 27 percent decrease in the phosphocreatine:ATP ratio in response to stress testing, whereas the woman whose results are shown in Figure 2B had a decrease of 1 percent. In both examples, it is evident that the decrease in the ratio was mostly due to a decline in phosphocreatine, since the ATP level tended to remain stable. The phosphocreatine:ATP ratio typically returned to pretesting values within 10 minutes after testing and returned to pretesting levels in all subjects within 20 minutes.We examined a number of risk factors — resting hemodynamic variables, hemodynamic response to stress testing, ejection fraction, thickness of the left ventricular wall, the results of radionuclide myocardial perfusion studies during stress testing, and response of brachial flow to stress testing — to gain further insight into the seven women with an abnormal decrease in the phosphocreatine:ATP ratio in response to stress testing (Table 1Table 1
Characteristics of Women with a Normal Response to Stress Testing and Women with an Abnormal Response.). There were no significant differences between this subgroup and the subgroup with a normal decrease in the phosphocreatine:ATP ratio in response to stress testing in any of the variables other than the phosphocreatine:ATP ratio. In addition, there was no correlation between the increase in the product of the heart rate and systolic blood pressure (rate–pressure product) and the change in the phosphocreatine:ATP ratio during stress testing.Discussion
Our results provide direct evidence of a myocardial metabolic change in women with chest pain and no angiographically significant coronary stenoses. One fifth of these women had an abnormal decrease in the myocardial phosphocreatine:ATP ratio during mild handgrip exercise. Interestingly, the magnitude of this decrease was equal to or greater than that in patients with stenosis of the left anterior descending coronary artery of at least 70 percent.
These results suggest that among women with chest pain but without coronary stenoses, a subgroup has metabolic evidence of myocardial ischemia during mild stress testing. The threshold we set for an abnormal response was 2 SD below the mean value for the reference population. Assuming a gaussian distribution, we estimate that 1 of 40 measurements (2.5 percent) should be below this threshold. Twenty percent of our patients had abnormal results. Since we measured the phosphocreatine:ATP ratio on a continuous scale, the threshold value can be adjusted after further refinement and verification. This may cause the threshold to shift upward, which would then shift the two patients with borderline results into the subgroup with abnormal responses, increasing the percentage of abnormal responses. Ultimately, with long-term follow-up, the prognostic value of this measurement can be assessed and compared with the value of other methods of identifying ischemia.
There are several potential physiologic and metabolic mechanisms for an abnormal decrease in the phosphocreatine:ATP ratio in response to stress testing in the absence of coronary stenoses, including microvascular coronary artery disease, coronary vasospasm, and elevation of left ventricular diastolic pressure (i.e., lusitropy). Microvascular coronary artery disease is usually assessed clinically by intracoronary Doppler ultrasonography, which shows an inadequate increase in flow in response to a direct-acting vasodilator such as adenosine or an endothelium-dependent vasodilator such as acetylcholine. Hasdai et al. recently reported that 20 subjects (10 of them women) with recurrent chest pain but no angiographically significant coronary stenoses had abnormal responses to acetylcholine.21 One third of these subjects had a reduced response of coronary blood flow to acetylcholine on Doppler ultrasonography, findings that correlated with independently assessed results of radionuclide perfusion studies. Other groups have reported similar impairments in coronary-artery responses to acetylcholine in patients with chest pain and normal coronary arteries, although none have directly measured coronary microvascular flow or provided metabolic evidence of myocardial ischemia in response to this abnormality.22-24
Coronary vasospasm is an uncommon response to exercise and is likely to be associated with chest pain and ST-segment elevation. Only two subjects (3 percent) in our study reported chest pain during stress testing. Lusitropy causes insufficient myocardial perfusion as a result of elevated left ventricular diastolic pressure. However, we found no significant difference in the prevalence of hypertension or the thickness of the left ventricular wall between the women with a normal decrease in the phosphocreatine:ATP ratio in response to stress testing and those with an abnormal decrease. Given the concordance between our results and those of others,21-24 the presence of microvascular coronary artery disease may best explain why the phosphocreatine:ATP ratio was abnormal during stress testing in women with chest pain but no angiographically significant coronary stenoses.
Myocardial 31P-NMR spectroscopy is a sensitive method of identifying ischemia and ischemic damage in a number of diseases.13-15 Bottomley et al. were the first to demonstrate that the resting phosphocreatine:ATP ratio was decreased in patients with myocardial infarction.13 Neubauer et al. found that the resting phosphocreatine:ATP ratio correlated with the clinical severity of myocardial dysfunction and that it increased after pharmacologic treatment.14 Weiss et al. reported a significant decrease in the phosphocreatine:ATP ratio during isometric handgrip exercise in patients with coronary stenoses of at least 70 percent.15 This ratio did not change significantly during exercise in either normal subjects or patients with nonischemic heart disease. In addition, of five patients with coronary stenoses of at least 70 percent and an abnormal decrease in the phosphocreatine:ATP ratio during isometric exercise, all had normal values during exercise after undergoing revascularization.
Yabe et al.16 reported a reduction in the phosphocreatine:ATP ratio during handgrip exercise among patients with ischemia but not among those without ischemia, with the use of thallium redistribution imaging as the standard for identifying ischemia. Thus, the body of literature on 31P-NMR spectroscopy to date strongly supports the hypothesis that decreases in the myocardial phosphocreatine:ATP ratio with handgrip exercise (which induces mild-to-moderate stress) provide direct metabolic evidence of the presence of myocardial ischemia.
The decrease in the phosphocreatine:ATP ratio during stress testing in our patients with angiographically significant coronary stenoses (mean decrease, 17.2 percent) was not as great as that reported by Weiss et al., who noted an average decrease of 35 percent among similar patients.15 Several factors in our technique might minimize such decreases. We averaged the measurements over a period of approximately eight minutes. A delay in the response of high-energy phosphates to stress would result in an artifactually larger phosphocreatine:ATP ratio. It is also possi-ble that the mild exercise test we used did not generate enough stress to induce an abnormal metabolic response. This explanation is unlikely, since there was no correlation between the increase in the rate–pressure product and the decrease in the phosphocreatine:ATP ratio. Thus, we may have underestimated the true prevalence of myocardial ischemia among women without angiographically significant coronary stenoses.
A major limitation of our approach was the inability to assess the phosphocreatine:ATP ratio in regions other than the anterior wall of the heart because of decreased sensitivity of the surface coil at depths of more than 10 cm. Hence, our results are relevant only with respect to the metabolic status of the anterior wall of the heart. A second limitation was the inability to measure inorganic phosphate accurately in vivo. Measurements of inorganic phosphate can provide a means of assessing pH on the basis of the chemical shift of the inorganic phosphate peak relative to that of phosphocreatine. With use of a magnetic field of 1.5 tesla, inorganic phosphate cannot be reliably measured, because of the overlap of the two peaks arising from the presence of 2,3-diphosphoglycerate in red cells. We plan to perform these experiments in a system with a stronger magnetic field. The improved spectral resolution of such a system will allow pH to be monitored and will identify the acidosis associated with ischemia.
A final limitation of our study was the lack of provocative coronary-vasospasm testing in our subjects, since primary epicardial coronary vasoconstriction is another possible mechanism of the abnormal phosphocreatine:ATP response. We believe that this explanation is unlikely, since none of our patients had ST-segment elevations typical of the presence of variant angina and previous studies in similar populations of patients with chest pain and no coronary stenoses have shown this pathophysiologic mechanism to be infrequent.21-24
In conclusion, we found that at least 20 percent of women who were undergoing coronary angiography to evaluate chest-pain syndromes in the absence of angiographically significant coronary-artery stenoses had evidence of altered myocardial metabolism on stress testing combined with 31P-NMR spectroscopy, suggesting the presence of ischemia. The concordance of our work with the findings of others using Doppler measurements of coronary-artery flow suggests that microvascular coronary artery disease is a likely mechanism for myocardial ischemia in the absence of angiographically significant stenoses. A noninvasive nontraumatic method to identify a metabolic abnormality in this subgroup of women with chest-pain syndromes may facilitate the development of treatment for this ubiquitous disease.
Supported by contracts (N01-HV-68161, N01-HV-68162, N01-HV-68163, and N01-HV-68164) with the National Heart, Lung, and Blood Institute, by a General Clinical Research Center grant (MO1-RR00425) from the National Center for Research Resources, and by grants from the Gustavus and Louis Pfeiffer Research Foundation, the Women's Guild of Cedars–Sinai Medical Center, the Ladies Hospital Aid Society of Western Pennsylvania, and QMED.
Source Information
From the Center for Nuclear Magnetic Resonance Research and Development (S.D.B., J.A.H., G.M.P.) and Division of Cardiovascular Disease, Department of Medicine (W.J.R., G.M.P.), University of Alabama at Birmingham, Birmingham; the Division of Cardiology, Department of Medicine, Cedars–Sinai Research Institute, Cedars–Sinai Medical Center, Los Angeles (C.N.B.M.); the Division of Cardiology, Department of Medicine, University of Florida, Gainesville (C.J.P.); the Division of Cardiology, Department of Medicine, Allegheny University of the Health Sciences, Pittsburgh (N.R.); the Division of Cardiology, Rhode Island Hospital, Providence (B.L.S.); and the Division of Cardiology, Department of Medicine (S.R.), and the Department of Epidemiology, Graduate School of Public Health (S.F.K.), University of Pittsburgh, Pittsburgh.
Address reprint requests to Dr. Pohost at the Center for NMR R&D, UAB, 828 8th Ct. S., Birmingham, AL 35294.
- References
References
1
Davis KB ,Chaitman B ,Ryan T ,Bittner V ,Kennedy JW . Comparison of 15-year survival for men and women after initial medical or surgical treatment for coronary artery disease: a CASS Registry study. J Am Coll Cardiol 1995;25:1000-1009
CrossRef | Web of Science | Medline2
Papanicolaou MN ,Califf RM ,Hlatky MA , et al. Prognostic implications of angiographically normal and insignificantly narrowed coronary arteries. Am J Cardiol 1986;58:1181-1187
CrossRef | Web of Science | Medline3
Kaski JC ,Rosano GM ,Collins P ,Nihoyannopoulos P ,Maseri A ,Poole-Wilson PA . Cardiac syndrome X: clinical characteristics and left ventricular function: long-term follow-up study. J Am Coll Cardiol 1995;25:807-814
CrossRef | Web of Science | Medline4
Likoff W ,Segal BL ,Kasparian H . Paradox of normal selective coronary arteriograms in patients considered to have unmistakable coronary heart disease. N Engl J Med 1967;276:1063-1066
Full Text | Web of Science | Medline5
Kemp HG ,Elliott WC ,Gorlin R . The anginal syndrome with normal coronary arteriography. Trans Assoc Am Physicians 1967;80:59-70
Medline6
Greenberg MA ,Grose RM ,Neuburger N ,Silverman R ,Strain JE ,Cohen MV . Impaired coronary vasodilator responsiveness as a cause of lactate production during pacing-induced ischemia in patients with angina pectoris and normal coronary arteries. J Am Coll Cardiol 1987;9:743-751
CrossRef | Web of Science | Medline7
Crake T ,Canepa-Anson R ,Shapiro L ,Poole-Wilson PA . Continuous recording of coronary sinus oxygen saturation during atrial pacing in patients with coronary artery disease or with syndrome X. Br Heart J 1988;59:31-38
CrossRef | Web of Science | Medline8
Camici P ,Marraccini P ,Lorenzoni R , et al. Metabolic markers of stress-induced myocardial ischemia. Circulation 1991;83:Suppl III:III-89
Schaefer S ,Camacho SA ,Gober J , et al. Response of myocardial metabolites to graded regional ischemia: 31P NMR spectroscopy of porcine myocardium in vivo. Circ Res 1989;64:968-976
Web of Science | Medline10
Schaefer S ,Schwartz GG ,Gober JR , et al. Relationship between myocardial metabolites and contractile abnormalities during graded regional ischemia: phosphorus-31 nuclear magnetic resonance studies of porcine myocardium in vivo. J Clin Invest 1990;85:706-713
CrossRef | Web of Science | Medline11
Nunnally RL ,Bottomley PA . Assessment of pharmacological treatment of myocardial infarction by phosphorus-31 NMR with surface coils. Science 1981;311:177-180
CrossRef | Web of Science12
Flaherty JT ,Weisfeldt ML ,Bulkley BH ,Gardner TJ ,Gott VL ,Jacobus WE . Mechanisms of ischemic myocardial cell damage assessed by phosphorus-31 nuclear magnetic resonance. Circulation 1982;65:561-570
CrossRef | Web of Science | Medline13
Bottomley PA ,Herfkens RJ ,Smith LS ,Bashore TM . Altered phosphate metabolism in myocardial infarction: P-31 MR spectroscopy. Radiology 1987;165:703-707
Web of Science | Medline14
Neubauer S ,Krahe T ,Schindler R , et al. 31P Magnetic resonance spectroscopy in dilated cardiomyopathy and coronary artery disease: altered cardiac high-energy phosphate metabolism in heart failure. Circulation 1992;86:1810-1818
Web of Science | Medline15
Weiss RG ,Bottomley PA ,Hardy CJ ,Gerstenblith G . Regional myocardial metabolism of high-energy phosphates during isometric exercise in patients with coronary artery disease. N Engl J Med 1990;323:1593-1600
Full Text | Web of Science | Medline16
Yabe T ,Mitsunami K ,Okada M ,Morikawa S ,Inubushi T ,Kinoshita M . Detection of myocardial ischemia by 31P magnetic resonance spectroscopy during handgrip exercise. Circulation 1994;89:1709-1716
Web of Science | Medline17
Merz CN ,Kelsey SF ,Pepine CJ , et al. The Women's Ischemia Syndrome Evaluation (WISE) study: protocol design, methodology and feasibility report. J Am Coll Cardiol 1999;33:1453-1461
CrossRef | Web of Science | Medline18
Summary of the second report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel II)
CrossRef | Web of Science19
Van de Bos A. Parameter estimation. In: Sydenham PH, ed. Handbook of measurement science. Vol. 1. Chichester, England: John Wiley, 1982.
20
Cramér H. Mathematical methods of statistics. Princeton, N.J.: Princeton University Press, 1946.
21
Hasdai D ,Gibbons RJ ,Holmes DR Jr ,Higano ST ,Lerman A . Coronary endothelial dysfunction in humans is associated with myocardial perfusion defects. Circulation 1997;96:3390-3395
Web of Science | Medline22
Ouyyumi AA ,Cannon RO III ,Panza JA ,Diodati JG ,Epstein SE . Endothelial dysfunction in patients with chest pain and normal coronary arteries. Circulation 1992;86:1864-1871
Web of Science | Medline23
Egashira K ,Inou T ,Hirooka Y ,Yamada A ,Urabe Y ,Takeshita A . Evidence of impaired endothelium-dependent coronary vasodilatation in patients with angina pectoris and normal coronary angiograms. N Engl J Med 1993;328:1659-1664
Full Text | Web of Science | Medline24
Egashira K ,Inou T ,Hirooka Y , et al. Impaired coronary blood flow response to acetylcholine in patients with coronary risk factors and proximal atherosclerotic lesions. J Clin Invest 1993;91:29-37
CrossRef | Web of Science | Medline
- Citing Articles (96)
Citing Articles
1
Ki E Park, Carl J Pepine. (2011) Microvascular dysfunction: what have we learned from WISE?. Expert Review of Cardiovascular Therapy 9:12, 1491-1494
CrossRef2
Cameron J. Holloway, Joseph Suttie, Sairia Dass, Stefan Neubauer. (2011) Clinical Cardiac Magnetic Resonance Spectroscopy. Progress in Cardiovascular Diseases 54:3, 320-327
CrossRef3
Islam A. Elsherbiny. (2011) Left Ventricular Function and Exercise Capacity in Patients with Slow Coronary Flow. Echocardiographyno-no
CrossRef4
Gert Klug, Ralf H. Zwick, Agnes Mayr, Michael F. Schocke, Peter Steinboeck, Werner Jaschke, Otmar Pachinger, Bernhard Metzler. (2011) Correlation of cardiovascular risk scores with myocardial high-energy phosphate metabolism. International Journal of Cardiology 150:2, 208-210
CrossRef5
Gerald Liew, Jie Jin Wang. (2011) Retinal Vascular Signs: A Window to the Heart?. Revista Española de Cardiología (English Edition) 64:6, 515-521
CrossRef6
A. H. E. M. Maas, Y. T. van der Schouw, V. Regitz-Zagrosek, E. Swahn, Y. E. Appelman, G. Pasterkamp, H. ten Cate, P. M. Nilsson, M. V. Huisman, H. C. G. Stam, K. Eizema, M. Stramba-Badiale. (2011) Red alert for women's heart: the urgent need for more research and knowledge on cardiovascular disease in women: Proceedings of the Workshop held in Brussels on Gender Differences in Cardiovascular disease, 29 September 2010. European Heart Journal 32:11, 1362-1368
CrossRef7
Gerald Liew, Jie Jin Wang. (2011) Manifestaciones vasculares retinianas: ¿reflejan el estado del corazón?. Revista Española de Cardiología 64:6, 515-521
CrossRef8
R. Scott Wright, Jeffrey L. Anderson, Cynthia D. Adams, Charles R. Bridges, Donald E. Casey, Steven M. Ettinger, Francis M. Fesmire, Theodore G. Ganiats, Hani Jneid, A. Michael Lincoff, Eric D. Peterson, George J. Philippides, Pierre Theroux, Nanette K. Wenger, James Patrick Zidar. (2011) 2011 ACCF/AHA Focused Update Incorporated Into the ACC/AHA 2007 Guidelines for the Management of Patients With Unstable Angina/Non–ST-Elevation Myocardial Infarction. Journal of the American College of Cardiology 57:19, e215-e367
CrossRef9
Mark R. Vesely, Vasken Dilsizian. (2011) Microvascular Angina: Assessment of Coronary Blood Flow, Flow Reserve, and Metabolism. Current Cardiology Reports 13:2, 151-158
CrossRef10
Anita V. Kusnoor, Angela D. Ferguson, Ruth Falik. (2011) Ischemic Heart Disease in Women: A Review for Primary Care Physicians. Southern Medical Journal 104:3, 200-204
CrossRef11
Lynn Nugent, Puja K. Mehta, C. Noel Bairey Merz. (2011) Gender and microvascular angina. Journal of Thrombosis and Thrombolysis 31:1, 37-46
CrossRef12
MATHEEN A. KHUDDUS, CARL J. PEPINE, EILEEN M. HANDBERG, C. NOEL BAIREY MERZ, GEORGE SOPKO, ANTHONY A. BAVRY, SCOTT J. DENARDO, SUSAN P. McGORRAY, KAREN M. SMITH, BARRY L. SHARAF, STEVEN J. NICHOLLS, STEVEN E. NISSEN, R. DAVID ANDERSON. (2010) An Intravascular Ultrasound Analysis in Women Experiencing Chest Pain in the Absence of Obstructive Coronary Artery Disease: A Substudy from the National Heart, Lung and Blood Institute-Sponsored Women's Ischemia Syndrome Evaluation (WISE). Journal of Interventional Cardiology 23:6, 511-519
CrossRef13
Gianluca Perseghin, Guido Lattuada, Francesco De Cobelli, Antonio Esposito, Tamara Canu, Francesca Ragogna, Paola Maffi, Paola Scifo, Antonio Secchi, Alessandro Del Maschio. (2010) Left ventricular function and energy homeostasis in patients with type 1 diabetes with and without microvascular complications. International Journal of Cardiology
CrossRef14
Padmini Varadarajan, Ramdas G. Pai, Krishna S. Nayak, Hee-Won Kim, Gerald M. Pohost. 2010. Cardiovascular Magnetic Resonance: Evaluation of Myocardial Function, Perfusion, and Viability. , 196-245.
CrossRef15
C. Leuzzi, M.G. Modena. (2010) Coronary artery disease: Clinical presentation, diagnosis and prognosis in women. Nutrition, Metabolism and Cardiovascular Diseases 20:6, 426-435
CrossRef16
C. Noel Bairey Merz, Marian B. Olson, Candace McClure, Yu-Ching Yang, James Symons, George Sopko, Sheryl F. Kelsey, Eileen Handberg, B. Delia Johnson, Rhonda M. Cooper-DeHoff, Barry Sharaf, William J. Rogers, Carl J. Pepine. (2010) A randomized controlled trial of low-dose hormone therapy on myocardial ischemia in postmenopausal women with no obstructive coronary artery disease: Results from the National Institutes of Health/National Heart, Lung, and Blood Institute–sponsored Women's Ischemia Syndrome Evaluation (WISE). American Heart Journal 159:6, 987.e1-987.e7
CrossRef17
W. Gregory Hundley, David A. Bluemke, J. Paul Finn, Scott D. Flamm, Mark A. Fogel, Matthias G. Friedrich, Vincent B. Ho, Michael Jerosch-Herold, Christopher M. Kramer, Warren J. Manning, Manesh Patel, Gerald M. Pohost, Arthur E. Stillman, Richard D. White, Pamela K. Woodard. (2010) ACCF/ACR/AHA/NASCI/SCMR 2010 Expert Consensus Document on Cardiovascular Magnetic Resonance. Journal of the American College of Cardiology 55:23, 2614-2662
CrossRef18
Yasushi Matsuzawa, Seigo Sugiyama, Koichi Sugamura, Toshimitsu Nozaki, Keisuke Ohba, Masaaki Konishi, Junichi Matsubara, Hitoshi Sumida, Koichi Kaikita, Sunao Kojima, Yasuhiro Nagayoshi, Megumi Yamamuro, Yasuhiro Izumiya, Satomi Iwashita, Kunihiko Matsui, Hideaki Jinnouchi, Kazuo Kimura, Satoshi Umemura, Hisao Ogawa. (2010) Digital Assessment of Endothelial Function and Ischemic Heart Disease in Women. Journal of the American College of Cardiology 55:16, 1688-1696
CrossRef19
Matthias G. Friedrich. (2010) Current status of cardiovascular magnetic resonance imaging in the assessment of coronary vasculature. Canadian Journal of Cardiology 26, 51A-55A
CrossRef20
Nico Merkle, Jochen Wöhrle, Thorsten Nusser, Olaf Grebe, Jochen Spiess, Jan Torzewski, Vinzenz Hombach. (2010) Diagnostic performance of magnetic resonance first pass perfusion imaging is equally potent in female compared to male patients with coronary artery disease. Clinical Research in Cardiology 99:1, 21-28
CrossRef21
Stefan Neubauer. 2010. Cardiovascular Magnetic Resonance Spectroscopy. , 556-568.
CrossRef22
Lucy E. Hudsmith, Damian J. Tyler, Yaso Emmanuel, Steffen E. Petersen, Jane M. Francis, Hugh Watkins, Kieran Clarke, Matthew D. Robson, Stefan Neubauer. (2009) 31P cardiac magnetic resonance spectroscopy during leg exercise at 3 Tesla. The International Journal of Cardiovascular Imaging 25:8, 819-826
CrossRef23
Hee-Won Kim, Don Lee, Gerald M Pohost. (2009) 31 P cardiovascular magnetic resonance spectroscopy: a unique approach to the assessment of the myocardium. Future Cardiology 5:6, 523-527
CrossRef24
Gabriele Fragasso, Sergio L. Chierchia, Francesco Arioli, Orazio Carandente, Stefano Gerosa, Mauro Carlino, Altin Palloshi, Luigi Gianolli, Giliola Calori, Ferruccio Fazio, Alberto Margonato. (2009) Coronary slow-flow causing transient myocardial hypoperfusion in patients with cardiac syndrome X: Long-term clinical and functional prognosis. International Journal of Cardiology 137:2, 137-144
CrossRef25
Paul A. Bottomley. 2009. NMR Spectroscopy of the Human Heart. .
CrossRef26
Richard O. Cannon. (2009) Microvascular Angina and the Continuing Dilemma of Chest Pain With Normal Coronary Angiograms. Journal of the American College of Cardiology 54:10, 877-885
CrossRef27
I.A.C. Vermeltfoort, P.G.H.M. Raijmakers, D.A.M. Odekerken, A.F.M. Kuijper, A. Zwijnenburg, G.J.J. Teule. (2009) Association between anxiety disorder and the extent of ischemia observed in cardiac syndrome X. Journal of Nuclear Cardiology 16:3, 405-410
CrossRef28
Aparna Singhal, Kalyanam Shivkumar, Amir Huda, M. Albert Thomas. (2009) Current status of cardiac MR spectroscopy. Progress in Nuclear Magnetic Resonance Spectroscopy 54:3-4, 255-277
CrossRef29
Sundeep Chaudhry, Ross Arena, Karlman Wasserman, James E. Hansen, Gregory D. Lewis, Jonathan Myers, Nicolas Chronos, William E. Boden. (2009) Exercise-Induced Myocardial Ischemia Detected by Cardiopulmonary Exercise Testing. The American Journal of Cardiology 103:5, 615-619
CrossRef30
F. Rollini, L. Mfeukeu, M.G. Modena. (2009) Assessing coronary heart disease in women. Maturitas 62:3, 243-247
CrossRef31
Tiong K. Lim, AnnaMaria J Choy, Faisel Khan, Jill JF Belch, Allan D Struthers, Chim C Lang. (2009) Therapeutic Development in Cardiac Syndrome X: A Need to Target the Underlying Pathophysiology. Cardiovascular Therapeutics 27:1, 49-58
CrossRef32
Amalia Peix, Aníbal González, Ernesto J. García, Juan Valiente, Lázaro O. Cabrera, Sherien Sixto, César E. Filgueiras, Beatriz Cabalé, Sheila Hechavarría, Iovank González, Regla Carrillo, David García-Barreto. (2009) Left Ventricular Dysfunction Secondary to Ischemia in Women with Angina and Normal Coronary Angiograms. Journal of Women's Health 18:2, 155-161
CrossRef33
Lucy E. Hudsmith, Stefan Neubauer. (2009) Magnetic Resonance Spectroscopy in Myocardial Disease. JACC: Cardiovascular Imaging 2:1, 87-96
CrossRef34
Adam Grzybowski, Wiesław Puchalski, Bozena Zieba, Marcin Gruchala, Marcin Fijalkowski, Katarzyna Storoniak, Wojciech Sobiczewski, Dariusz Ciecwierz, Radoslaw Targonski, Andrzej Rynkiewicz. (2008) How to improve noninvasive coronary artery disease diagnostics in premenopausal women?. American Heart Journal 156:5, 964.e1-964.e5
CrossRef35
Fadi Alqaisi, Firas AlBadarin, Zehra Jaffery, Leonidas Tzogias, Muath Dawod, Gordon Jacobsen, Karthik Ananthasubramaniam. (2008) Prognostic predictors and outcomes in patients with abnormal myocardial perfusion imaging and angiographically insignificant coronary artery disease. Journal of Nuclear Cardiology 15:6, 754-761
CrossRef36
Paul R. Slobodny. (2008) Cardiac Syndrome X. Dimensions of Critical Care Nursing 27:5, 209-212
CrossRef37
Lucy E Hudsmith, Stefan Neubauer. (2008) Detection of myocardial disorders by magnetic resonance spectroscopy. Nature Clinical Practice Cardiovascular Medicine 5, S49-S56
CrossRef38
B. J. Kim, S.-H. Lee, B. S. Kang, B.-W. Yoon, J.-K. Roh. (2008) Diabetes increases large artery diseases, but not small artery diseases in the brain. Journal of Neurology 255:8, 1176-1181
CrossRef39
R Kent Hermsmeyer, Theresa L Thompson, Gerald M Pohost, Juan Carlos Kaski. (2008) Cardiovascular effects of medroxyprogesterone acetate and progesterone: a case of mistaken identity?. Nature Clinical Practice Cardiovascular Medicine 5:7, 387-395
CrossRef40
Amanda A. Fox. (2008) Pro: Newly Appreciated Pathophysiology of Ischemic Heart Disease in Women Mandates Changes in Perioperative Management. Anesthesia & Analgesia 107:1, 29-32
CrossRef41
Igor Klem, Simon Greulich, John F. Heitner, Han Kim, Holger Vogelsberg, Eva-Maria Kispert, Srivani R. Ambati, Christian Bruch, Michele Parker, Robert M. Judd, Raymond J. Kim, Udo Sechtem. (2008) Value of Cardiovascular Magnetic Resonance Stress Perfusion Testing for the Detection of Coronary Artery Disease in Women. JACC: Cardiovascular Imaging 1:4, 436-445
CrossRef42
Kevin McGeechan, Gerald Liew, Petra Macaskill, Les Irwig, Ronald Klein, A. Richey Sharrett, Barbara E.K. Klein, Jie J. Wang, Lloyd E. Chambless, Tien Y. Wong. (2008) Risk Prediction of Coronary Heart Disease Based on Retinal Vascular Caliber (from the Atherosclerosis Risk In Communities [ARIC] Study). The American Journal of Cardiology 102:1, 58-63
CrossRef43
Karin H. Humphries, Aihua Pu, Min Gao, Ronald G. Carere, Louise Pilote. (2008) Angina with “normal” coronary arteries: Sex differences in outcomes. American Heart Journal 155:2, 375-381
CrossRef44
Narbeh Melikian, Bernard De Bruyne, William F. Fearon, Philip A. MacCarthy. (2008) The Pathophysiology and Clinical Course of the Normal Coronary Angina Syndrome (Cardiac Syndrome X). Progress in Cardiovascular Diseases 50:4, 294-310
CrossRef45
Gianluca Perseghin, Guido Lattuada, Francesco De Cobelli, Antonio Esposito, Elena Belloni, Georgia Ntali, Francesca Ragogna, Tamara Canu, Paola Scifo, Alessandro Del Maschio, Livio Luzi. (2008) Increased mediastinal fat and impaired left ventricular energy metabolism in young men with newly found fatty liver. Hepatology 47:1, 51-58
CrossRef46
Dudley J. Pennell. (2008) Perfusion Abnormality, Normal Coronaries, and Chest Pain
Editorials published in the Journal of the American College of Cardiology reflect the views of the authors and do not necessarily represent the views of JACC or the American College of Cardiology.. Journal of the American College of Cardiology 51:4, 473-475
CrossRef47
Gaetano A. Lanza, Antonino Buffon, Alfonso Sestito, Luigi Natale, Gregory A. Sgueglia, Leda Galiuto, Fabio Infusino, Luca Mariani, Antonio Centola, Filippo Crea. (2008) Relation Between Stress-Induced Myocardial Perfusion Defects on Cardiovascular Magnetic Resonance and Coronary Microvascular Dysfunction in Patients With Cardiac Syndrome X. Journal of the American College of Cardiology 51:4, 466-472
CrossRef48
Amgad N. Makaryus, Leslee J. Shaw, Jennifer H. Mieres. (2007) Diagnostic Strategies for Heart Disease in Women. Cardiology in Review 15:6, 279-287
CrossRef49
Giovanni Storto, Anna Rita Sorrentino, Teresa Pellegrino, Raffaele Liuzzi, Mario Petretta, Alberto Cuocolo. (2007) Assessment of coronary flow reserve by sestamibi imaging in patients with typical chest pain and normal coronary arteries. European Journal of Nuclear Medicine and Molecular Imaging 34:8, 1156-1161
CrossRef50
Jeffrey L. Anderson, Cynthia D. Adams, Elliott M. Antman, Charles R. Bridges, Robert M. Califf, Donald E. Casey, William E. Chavey, Francis M. Fesmire, Judith S. Hochman, Thomas N. Levin, A. Michael Lincoff, Eric D. Peterson, Pierre Theroux, Nanette Kass Wenger, R. Scott Wright, Sidney C. Smith, Alice K. Jacobs, Cynthia D. Adams, Jeffrey L. Anderson, Elliott M. Antman, Jonathan L. Halperin, Sharon A. Hunt, Harlan M. Krumholz, Frederick G. Kushner, Bruce W. Lytle, Rick Nishimura, Joseph P. Ornato, Richard L. Page, Barbara Riegel. (2007) ACC/AHA 2007 Guidelines for the Management of Patients With Unstable Angina/Non–ST-Elevation Myocardial Infarction. Journal of the American College of Cardiology 50:7, e1-e157
CrossRef51
Amalia Peix, Ernesto J. Garc??a, Juan Valiente, Francisco Torn??s, L??zaro O. Cabrera, Beatriz Cabal??, Regla Carrillo, David Garc??a-Barreto. (2007) Ischemia in women with angina and normal coronary angiograms. Coronary Artery Disease 18:5, 361-366
CrossRef52
C. Noel Bairey Merz, Wafia Eteiba, Carl J. Pepine, B. Delia Johnson, Leslee J. Shaw, Sheryl F. Kelsey. (2007) Cardiac syndrome X: Relation to microvascular angina and other conditions. Current Cardiovascular Risk Reports 1:2, 167-175
CrossRef53
Gerald M Pohost, Krishna S. Nayak. 2006. CMR: The Future. , 425-434.
CrossRef54
Steven M. Stevens, Hee-Won Kim, Gerald M. Pohost. 2006. Ischemic Heart Disease: Myocardial Metabolism. , 195-212.
CrossRef55
Uzma Iqbal, Anthony R Fuisz. 2006. Cardiomyopathies. , 257-274.
CrossRef56
Vera Regitz-Zagrosek. (2006) Therapeutic implications of the gender-specific aspects of cardiovascular disease. Nature Reviews Drug Discovery 5:5, 425-239
CrossRef57
Ramdas G. Pai, Padmini Varadarajan. (2006) Echocardiography and cardiovascular magnetic resonance: Evolution as complementary imaging tools. Current Cardiology Reports 8:3, 155-157
CrossRef58
Koichi Ochiai, Qingsong Hu, Joseph Lee, Abdul Mansoor, Jingbo Liu, Xiaohong Wang, Guangrong Gong, Yo Murakami, Yukada Ishibashi, Toshio Shimada, Jianyi Zhang. (2006) Functional and Bioenergetic Consequences of AT1 Antagonist Olmesartan Medoxomil in Hearts With Postinfarction LV Remodeling. Journal of Cardiovascular Pharmacology 47:5, 686-694
CrossRef59
Magda Heras. (2006) Cardiopatía isquémica en la mujer: presentación clínica, pruebas diagnósticas y tratamiento de los síndromes coronarios agudos. Revista Española de Cardiología 59:4, 371-381
CrossRef60
Ignacio Gil-Ortega, Raquel Marzoa Rivas, Ramón Ríos Vázquez, Juan Carlos Kaski. (2006) Role of inflammation and endothelial dysfunction in the pathogenesis of cardiac syndrome X. Future Cardiology 2:1, 63-73
CrossRef61
Bina Ahmed, C Noel Bairey Merz, George Sopko. (2006) Are we ‘WISE’r? Findings from the NHLBI-sponsored Women’s Ischemia Syndrome Evaluation study. Women's Health 2:1, 57-64
CrossRef62
Koichi Chida, Hiroki Otani, Masahiro Kohzuki, Haruo Saito, Yutaka Kagaya, Yoshihiro Takai, Shoki Takahashi, Shogo Yamada, Masayuki Zuguchi. (2006) The Relationship between Plasma BNP Level and the Myocardial Phosphocreatine/Adenosine Triphosphate Ratio Determined by Phosphorus-31 Magnetic Resonance Spectroscopy in Patients with Dilated Cardiomyopathy. Cardiology 106:3, 132-136
CrossRef63
Serkan Cay, Funda Biyikoglu, Gokhan Cihan, Sule Korkmaz. (2005) Mean Platelet Volume in the Patients with Cardiac Syndrome X. Journal of Thrombosis and Thrombolysis 20:3, 175-178
CrossRef64
Juraj Madaric, Jozef Bartunek, Katia Verhamme, Martin Penicka, Eddy Van Schuerbeeck, Paul Nellens, Guy R. Heyndrickx, William Wijns, Marc Vanderheyden, Bernard De Bruyne. (2005) Hyperdynamic Myocardial Response to Beta-Adrenergic Stimulation in Patients With Chest Pain and Normal Coronary Arteries. Journal of the American College of Cardiology 46:7, 1270-1275
CrossRef65
E. A. Asbury, P. Collins. (2005) Cardiac syndrome X. International Journal of Clinical Practice 59:9, 1063-1069
CrossRef66
Donna M. Polk, Tasneem Z. Naqvi. (2005) Cardiovascular disease in women: Sex differences in presentation, risk factors, and evaluation. Current Cardiology Reports 7:3, 166-172
CrossRef67
Tarang Ray, Robert W. Biederman, Mark Doyle, Sunil Mankad. (2005) Magnetic resonance imaging in the assessment of coronary artery disease. Current Atherosclerosis Reports 7:2, 108-114
CrossRef68
A.L. Pasqui, L. Puccetti, M. Di Renzo, F. Bruni, A. Camarri, A. Palazzuoli, F. Biagi, M. Servi, D. Bischeri, A. Auteri, M. Pastorelli. (2005) Structural and functional abnormality of systemic microvessels in cardiac syndrome X. Nutrition, Metabolism and Cardiovascular Diseases 15:1, 56-64
CrossRef69
W Brian Hyslop, Richard C Semelka. (2005) Future Directions in Body Magnetic Resonance Imaging. Topics in Magnetic Resonance Imaging 16:1, 3-14
CrossRef70
Riccardo Bigi, Lauro Cortigiani, Dario Gregori, Benedetta De Chiara, Oberdan Parodi, Cesare Fiorentini. (2004) Exercise versus recovery electrocardiography for predicting outcome in hypertensive patients with chest pain. Journal of Hypertension 22:11, 2193-2199
CrossRef71
A Chaudhuri, P.O Behan. (2004) In vivo magnetic resonance spectroscopy in chronic fatigue syndrome. Prostaglandins, Leukotrienes and Essential Fatty Acids 71:3, 181-183
CrossRef72
Patricia M Davidson, John Daly, Karen Hancock, Debra Jackson. (2004) Australian women and heart disease: Trends, epidemiological perspectives and the need for a culturally competent research agenda. Contemporary Nurse 16:1-2, 62-73
CrossRef73
Mark Doyle, Robert W. W. Biederman. (2004) Future prospects in magnetic resonance imaging. Current Cardiology Reports 6:1, 70-75
CrossRef74
Juan Carlos Kaski, Guillermo Aldama, Juan Cos??n-Sales. (2004) Cardiac Syndrome X. American Journal of Cardiovascular Drugs 4:3, 179-194
CrossRef75
Gerald M. Pohost, John R. Forder. (2003) From the atomic nucleus to man. Journal of the American College of Cardiology 42:9, 1594-1595
CrossRef76
Sunil Mankad, Ramzi Khalil, Christopher M. Kramer. (2003) MRI for the diagnosis of myocardial ischemia and viability. Current Opinion in Cardiology 18:5, 351-356
CrossRef77
R. G. IJzerman, R. T. de Jongh, M. A. M. Beijk, M. M. van Weissenbruch, H. A. Delemarre-van de Waal, E. H. Serne, C. D. A. Stehouwer. (2003) Individuals at increased coronary heart disease risk are characterized by an impaired microvascular function in skin. European Journal of Clinical Investigation 33:7, 536-542
CrossRef78
John R. Forder, Gerald M. Pohost. (2003) Cardiovascular nuclear magnetic resonance: basic and clinical applications. Journal of Clinical Investigation 111:11, 1630-1639
CrossRef79
Juan Cosín-Sales, Carmine Pizzi, Sue Brown, Juan Carlos Kaski. (2003) C-reactive protein, clinical presentation, and ischemic activity in patients with chest pain and normal coronary angiograms. Journal of the American College of Cardiology 41:9, 1468-1474
CrossRef80
Mark Doyle, Robert W. W. Biederman. (2003) Future prospects in cardiac magnetic resonance imaging. Current Cardiology Reports 5:1, 83-90
CrossRef81
Stefan Neubauer. (2003) Cardiac magnetic resonance spectroscopy. Current Cardiology Reports 5:1, 75-82
CrossRef82
Pamela Charney. (2002) Journal of Cardiovascular Risk 9:6, 303-307
CrossRef83
(2002) Cardiac Syndrome X. New England Journal of Medicine 347:17, 1377-1379
Full Text84
Panting, Jonathan R., Gatehouse, Peter D., Yang, Guang-Zhong, Grothues, Frank, Firmin, David N., Collins, Peter, Pennell, Dudley J., . (2002) Abnormal Subendocardial Perfusion in Cardiac Syndrome X Detected by Cardiovascular Magnetic Resonance Imaging. New England Journal of Medicine 346:25, 1948-1953
Full Text85
Shoji Yamamoto, Thomas N. James, Keishiro Kawamura, Masakiyo Nobuyoshi. (2002) Cardiocytic apoptosis and capillary endothelial swellingas morphological evidence of myocardial ischemia in ventricular biopsies from patients with angina and normal coronary arteriograms. Coronary Artery Disease 13:1, 25-35
CrossRef86
Steven P Schulman, David R Thiemann, Pamela Ouyang, Nisha C Chandra, Douglas S Schulman, Steven E Reis, Michael Terrin, Sandra Forman, Cicero Piva de Albuquerque, Raymond D Bahr, Susan N Townsend, Rosalie Cosgriff, Gary Gerstenblith. (2002) Effects of acute hormone therapy on recurrent ischemia in postmenopausal women with unstable angina. Journal of the American College of Cardiology 39:2, 231-237
CrossRef87
Rebecca C. Thurston, Francis J. Keefe, Laurence Bradley, K.Ranga Rama Krishnan, David S. Caldwell. (2001) Chest pain in the absence of coronary artery disease: a biopsychosocial perspective. Pain 93:2, 95-100
CrossRef88
Jassim Al Suwaidi, Stuart T. Higano, David R. Holmes, Amir Lerman. (2001) Pathophysiology, Diagnosis, and Current Management Strategies for Chest Pain in Patients With Normal Findings on Angiography. Mayo Clinic Proceedings 76:8, 813-822
CrossRef89
J Al Suwaidi, S T Higano, D R Holmes, A Lerman. (2001) Pathophysiology, diagnosis, and current management strategies for chest pain in patients with normal findings on angiography.. Mayo Clinic Proceedings 76:8, 813-822
CrossRef90
Eugenio Picano, Attila Pálinkás, Robert Amyot. (2001) Diagnosis of myocardial ischemia in hypertensive patients. Journal of Hypertension 19:7, 1177-1183
CrossRef91
Christopher R deFilippi, Salvatore Rosanio, Monica Tocchi, Rohit J Parmar, Marjorie A Potter, Barry F Uretsky, Marschall S Runge. (2001) Randomized comparison of a strategy of predischarge coronary angiography versus exercise testing in low-risk patients in a chest pain unit: in-hospital and long-term outcomes. Journal of the American College of Cardiology 37:8, 2042-2049
CrossRef92
Thomas Rutledge, Steven E Reis, Marian Olson, Jane Owens, Sheryl F Kelsey, Carl J Pepine, Nathaniel Reichek, William J Rogers, C.Noel Bairey Merz, George Sopko, Carol E Cornell, Barry Sharaf, Karen A Matthews. (2001) History of anxiety disorders is associated with a decreased likelihood of angiographic coronary artery disease in women with chest pain: the WISE study. Journal of the American College of Cardiology 37:3, 780-785
CrossRef93
Lizzy M. Brewster, Joseph F. Clark, Gert A. van Montfrans. (2000) Is greater tissue activity of creatine kinase the genetic factor increasing hypertension risk in black people of sub-Saharan African descent?. Journal of Hypertension 18:11, 1537-1544
CrossRef94
(2000) Chest Pain and Normal Coronary Arteries. New England Journal of Medicine 343:7, 511-512
Full Text95
(2000) Current Awareness. NMR in Biomedicine 13:5, 314-319
CrossRef96
Cannon, Richard O. III, Balaban, Robert S., . (2000) Chest Pain in Women with Normal Coronary Angiograms. New England Journal of Medicine 342:12, 885-887
Full Text
- Letters
