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J Am Coll Cardiol, 1999; 33:1056-1061
© 1999 by the American College of Cardiology Foundation
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CLINICAL STUDIES

Enhanced exercise-induced hyperkalemia in patients with syndrome X

Hans Erik Bøtker, MD, PhD*, Helle Sauer Sonne, MD*, Ole Frøbert, MD, PhD* and Frederik Andreasen, MD, PhD{dagger}

* Department of Cardiology, Skejby Hospital, University Hospital Aarhus, Aarhus, Denmark
{dagger} Department of Clinical Pharmacology, Institute of Pharmacology, University of Aarhus, Aarhus, Denmark

Manuscript received April 27, 1998; revised manuscript received October 26, 1998, accepted December 17, 1998.

Reprint requests and correspondence: Hans Erik Bøtker, MD, PhD, Department of Cardiology, Skejby Hospital/University Hospital Aarhus, Brendstrupgaardsvej, DK-8200 Aarhus N, Denmark


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
OBJECTIVES

The purpose of this study was to determine whether patients with syndrome X have altered potassium metabolism.

BACKGROUND

Patients with syndrome X have angina pectoris and exercise induced ST segment depression on the electrocardiogram despite normal coronary angiograms. Increasing evidence suggests that myocardial ischemia is uncommon in these patients. Altered potassium metabolism causing interstitial potassium accumulation in the myocardium may be an alternative mechanism for chest pain and ST segment depression in syndrome X.

METHODS

We compared the magnitude of exercise-induced hyperkalemia in 16 patients with syndrome X (12 female and four male, mean ± SD age 53 ± 6 years) and 15 matched healthy control subjects. The participants underwent a bicycle test at a fixed load of 75 W for 10 min, and blood samples were taken for analysis of potassium, catecholamines and lactate before, during and in the recovery period after exercise. In five patients with syndrome X, the test was repeated during alpha1 adrenoceptor blockade.

RESULTS

Baseline concentrations of serum potassium, plasma catecholamines and plasma lactate were similar in patients and control subjects. The rate of exercise-induced increment of serum potassium was increased in the patients (70 ± 29 vs. 30 ± 21 µmol/liter/min in control subjects, p < 0.001). Six patients, who stopped before 10 min of exercise, showed very rapid increments in serum potassium concentration. Compared to the control subjects, patients also demonstrated larger increments in rate–pressure product, plasma norepinephrine and lactate concentrations during exercise. The rate of serum potassium increment correlated with the rate of plasma norepinephrine increment in the patients (r = 0.63, p < 0.02), but not in the control subjects (r = 0.01, p = 0.97). Blockade of alpha1 adrenoceptors decreased systolic blood pressure at baseline, but did not influence the increment of serum potassium, plasma catecholamines and lactate.

CONCLUSIONS

Patients with syndrome X have enhanced exercise induced hyperkalemia in parallel with augmented increases of circulating norepinephrine and lactate. The prevailing mechanisms behind the abnormal potassium handling comprise sources distinct from alpha1-adrenoceptor activation.

Abbreviations and Acronyms
  ATPase = adenosine triphosphatase
  ECG = electrocardiogram
  EGTA = ethylene glycol tetraacetic acid
  VO2 peak = peak oxygen uptake

The cardiologic syndrome X is characterized by angina pectoris and ST segment depression during exercise testing but normal coronary arteries at angiography. Increasing evidence suggests that myocardial ischemia is uncommon in these patients (1,2). It has been proposed that potassium metabolism is altered in patients with syndrome X (3). Potassium is released from the human myocardium under conditions of stress or increases of heart rate (4). On cessation of tachycardia the small net loss of intracellular potassium is replaced to maintain a steady state. If patients with syndrome X release a greater amount of intracellular potassium or take up potassium more slowly, then potassium could be retained in the myocardium. Such an accumulation would account for features of syndrome X, including chest pain, ST segment changes, modification of coronary (5) and systemic vasoreactivity (6) and a good prognosis (7). However, no confirmatory data exist to support this hypothesis. Potassium regulation during exercise may reflect disturbances of potassium metabolism, because patients with syndrome X in addition to angina pectoris often suffer from generalized fatigue in the skeletal muscles (8). To determine whether there is any evidence of a disturbed potassium metabolism in patients with syndrome X we compared exercise-induced hyperkalemia in patients with syndrome X and matched healthy control subjects.


   Methods
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 Abstract
 Methods
Results
 Discussion
 References
 
Subjects.   We studied 16 patients with syndrome X (typical effort angina, ≥0.1 mV ST segment depression on bicycle exercise testing and normal coronary angiograms) (Table 1). Mean duration of symptoms was 4.2 years (range 6 months to 12 years). All patients were otherwise healthy, and none had concomitant cardiovascular or metabolic disease. Epicardial spasm was excluded by a hyperventilation test. Valvular and myocardial diseases were excluded by echocardiography and ventriculography. Ejection fraction was >55% in all patients. Prior to the study 12 patients were treated with calcium channel blocking agents, three with beta-adrenergic blocking agents and 16 with long-acting nitroglycerin.


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  		Table 1 Characteristics of Participants

 
Healthy control subjects were recruited among the hospital staff and blood donors. They were matched to the patients for age, gender, body mass index, maximal oxygen uptake and blood pressure. None of the volunteers had a history of neurologic, endocrinologic or cardiologic diseases. All were free of medication, and had a normal clinical investigation and a normal exercise electrocardiogram (ECG).

Study design.   The study was approved by the local Ethics Committee. All medications were discontinued two weeks before the study. Short-acting nitrates, however, were allowed up to 6 h before the study. Investigations were performed on two separate days within one week. At the first visit, participants underwent exercise ECG testing. Maximal aerobic capacity was expressed as peak oxygen uptake (VO2 peak) (9). During a separate visit, the participants underwent a bicycle test at a fixed load of 75 W for 10 min. A computer-connected Schiller ERGOMETRIC 900 bicycle ergometer and a Schiller Cardiovit CS-6/12 Exec mingograph (Geneva, Switzerland) were used. Blood pressure was measured automatically by a BOSCH EBM blood pressure measure unit (Berlin, Germany) connected to the computer. On the basis of the caloric coefficient of oxygen uptake of 13.95 ml/min per watt (10), individual oxygen uptake was extrapolated from workload as:

where W is the workload obtained and 3.5 resting oxygen consumption in ml/kg/min (11). A short catheter was inserted into a large antecubital vein. The system was kept patent by slow infusion of isotonic saline. Serum potassium and albumin were measured at baseline, every 2.5 min during the exercise test and at 1, 2, 3, 5, 7 and 10 min after cessation of the bicycle test. Plasma epinephrine, plasma norepinephrine and plasma lactate were measured before and at the end of exercise. Analysis for serum potassium was done with a standard method on a Kodak Ektachem 700 XR analyzer (Rochester, New York). For determination of epinephrine and norepinephrine 4 ml of blood was collected into glass tubes containing 80 µl ethylene glycol tetraacetic acid (EGTA)/gluthation (76 mg EGTA and 6 mg glutathion in 1 ml water, pH adjusted at 7.3). Samples were centrifuged and stored at –80°C until analysis. Analyses were performed using high performance liquid chromatography (12). Blood samples for determination of lactate were collected into heparinized ice-cooled glass tubes, centrifuged, deproteinized and stored at –80°C until later duplicate analysis. Plasma lactate was determined enzymatically using lactate dehydrogenase at pH = 9.0 (13).

The study was repeated in five patients after administration of an alpha1 adrenoceptor antagonist, doxazosin (Carduran) 2 mg orally 2 h before the test.

Statistical methods.   Data are presented as mean ± SD. Mean values are compared using paired and unpaired t tests. Correlations are assessed by linear regression analysis. A p value <0.05 is considered statistically significant.


   Results
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 Abstract
 Methods
 Results
Discussion
 References
 
Baseline serum potassium, plasma lactate, epinephrine and norepinephrine concentrations were similar in patients and control subjects (Table 2). Six patients with syndrome X terminated exercise testing before 10 min of exercise due to anginal pain. The individual increases of serum potassium during exercise in these patients are depicted in Figure 1, which also shows that the exercise-induced hyperkalemia is enhanced in the remaining syndrome X patients compared to the control subjects.


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  		Table 2 Baseline Data and Exercise Responses of Rate–Pressure Product, Serum-Potassium, Plasma Epinephrine, Plasma Norepinephrine and Plasma Lactate in Control Subjects and Patients With Syndrome X

 


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  		Figure 1 Changes in plasma potassium concentration (means ± SD) during exercise and in the recovery period after exercise in 10 patients with syndrome X (solid circles) and 16 matched control subjects (open circles). Changes in six patients who stopped before 10 min of exercise are shown individually (triangles). *p < 0.05 versus control subjects.

 
Absolute values of VO2 during exercise did not differ between patients and control subjects (18.7 ± 2.0 and 20.1 ± 2.6 ml/kg/min, p = 0.11). However, the relative value of the actual VO2 during the fixed workload in percentage of VO2 peak was significantly higher in the patients than in the control subjects (76 ± 14% vs. 63 ± 16%, p < 0.05). Correction for variations in relative submaximal effort by calculating the ratio of [rate of serum potassium increment/VO2 during fixed workload in proportion to VO2 peak] showed that the difference in the rate of serum potassium increment between patients and control subjects persisted (91 ± 27 vs. 51 ± 34 µmol/liter/min, p < 0.001).

During exercise, patients with syndrome X revealed larger increments in rate–pressure product, plasma norepinephrine and lactate concentrations than control subjects (Table 2). Four patients had ST segment depressions ≥0.1 mV at the termination of exercise. Among these one patient stopped exercise after 5 min and 10 s, whereas the remaining three patients completed the 10-min exercise scheme. No significant correlations were observed between the rate of potassium increment and rate of lactate increment in patients (r = 0.42, p = 0.11) or control subjects (r = 0.08, p = 0.77). In the patient group, the rate of potassium increment correlated with the rate of norepinephrine increment (r = 0.63, p < 0.02), whereas no correlation was found in control subjects (r = 0.01, p = 0.97). In the recovery period, the rate of serum potassium decrease did not differ between patients and control subjects (31 ± 19 and 38 ± 20 mmol/liter/min, p = 0.30).

After doxazosin administration to five of the patients who completed 10 min of bicycling during the first test, systolic blood pressure at baseline was decreased compared to the test without doxazosin (Table 3). Baseline plasma concentrations of potassium, epinephrine, norepinephrine and lactate were unchanged after doxazosin. During exercise the increase in rate–pressure product was unchanged with doxazosin, whereas the increases of plasma catecholamines tended to be higher after doxazosin administration. The increases in potassium and lactate were similar with and without doxazosin.


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  		Table 3 Baseline Data and Exercise Responses of Rate–Pressure Product, Serum Potassium, Plasma Epinephrine, Plasma Norepinephrine and Plasma Lactate in Five Patients With Syndrome X Before and After Doxazosin Administration

 

   Discussion
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 Abstract
 Methods
 Results
 Discussion
References
 
The present study shows that patients with syndrome X exhibit enhanced exercise-induced hyperkalemia in parallel with augmented increases of circulating norepinephrine and lactate concentrations compared to a matched group of healthy control subjects. The enhanced exercise-induced hyperkalemia in patients with syndrome X is not modulated by the alpha1 adrenergic antagonist doxazosin.

Potassium regulation.   Acute potassium homeostasis is controlled by extrarenal tissues and determined by epinephrine, norepinephrine and insulin (14). The abnormal potassium handling in patients with syndrome X is thought to affect the transport of potassium between intracellular and extracellular myocardial compartments and therefore involves components responsible for the acute regulation of potassium balance (15). Assessment of myocardial potassium exchange by determination of potassium concentrations in the coronary sinus is suboptimal because the measured changes may be small (2).

The skeletal muscles contain the largest pool of potassium in the body (75% of total) (14). The regulatory mechanisms of transsarcolemmal exchange of potassium in skeletal muscle and cardiac muscle are similar and appear to involve identical structures (16). Thus, we chose to study the acute regulation of potassium metabolism during exercise. We used a moderate workload (on average 70% of peak VO2) for a limited duration because it represents an integral part of the lifestyle in many adults and produces a predictable yet modest increase in the serum potassium concentration (17). We used the same absolute workload in all participants because the peak concentrations of potassium in plasma during exercise are proportional to exercise intensity, contracting muscle mass and the level of physical capacity (18,19). Syndrome X patients are expected to have compromised physical capacity because exercise induces angina pectoris. Thus, we sought to eliminate these confounders by selecting the control group to match the patient group as closely as possible with respect to body mass index and VO2 peak. Even so, the relative value of VO2 during the fixed workload in percentage of VO2 peak was, on average, higher in the patients than in the control subjects. These findings suggest that this workload is closer to the anaerobic threshold in the patients than in the control subjects (20), so that the enhanced hyperkalemia during exercise may be associated with a reduction of aerobic capacity. However, ratios for rate of potassium increments/VO2 during fixed workload in percentage of VO2 peak showed that the difference in exercise-induced hyperkalemia persisted after correction for individual variations in relative submaximal effort.

Exercise, catecholamines and insulin.   The main cellular mechanism regulating exercise-induced hyperkalemia is the Na+,K+, adenosine triphosphatase (ATPase) in skeletal muscle (14). The concentration of Na+,K+,ATPase exceeds the demands for Na+–K+ transport under usual physiologic conditions (14), and it is generally accepted that increased activation of the Na+,K+,ATPase is responsible for the reduction of exercise-induced hyperkalemia. Catecholamines increase K+ influx and Na+ efflux through selective beta2 adrenoceptor stimulation (17). Several studies have indicated that sympathetic activity in patients with syndrome X is increased (21–23). The results of the present study show that the enhanced exercise-induced hyperkalemia in patients with syndrome X occurs despite a simultaneously augmented increase in plasma norepinephrine. Moreover, the increase in norepinephrine and the increase in potassium correlated in the patients. This observation, together with previous observations that alpha-adrenergic stimulation causes an elevation of plasma potassium concentration (24,25), which can be reversed by phentolamine, an alpha-receptor antagonist, prompted us to study the influence of doxazosin, a selective alpha1 adrenoceptor antagonist, on exercise-induced hyperkalemia. Doxazosin increases the coronary flow reserve in patients with syndrome X (26). Assessed by the significant hemodynamic effect of doxazosin at rest, we achieved sufficient alpha1 blockade, but the hyperkalemic response during exercise was not modified. This finding tends to exclude a significant involvement of alpha1 adrenoceptor activation in the enhanced exercise-induced hyperkalemia in patients with syndrome X. At present, it is unknown whether the effect of alpha-adrenergic modification of potassium homeostasis is mediated via the alpha1 or alpha2 receptor. Because unspecific alpha-adrenoceptor blockade with phentolamine diminishes the exercise-induced rise in plasma potassium concentration in healthy subjects (27), we cannot exclude the possibility that an effect is mediated through the alpha2 receptor.

Insulin reduces the circulating potassium concentration by stimulation of the Na+,K+,ATPase in skeletal muscle. Patients with syndrome X are characterized by impaired insulin-stimulated glucose uptake in skeletal and cardiac muscle (28), but the actions of insulin on cellular glucose and potassium uptake are independent of one another (29,30). We have recently demonstrated that potassium handling in response to insulin is similar in patients with syndrome X and control subjects (28). Thus, insulin is not likely to be involved in the abnormal potassium handling during exercise in patients with syndrome X.

Limitations.   Although high extracellular concentrations of potassium are associated with ST segment depressions similar to those observed in the present study during exercise, the maximal serum potassium concentrations observed here were far from the serum concentrations of 8 to 12 mmol/liter that cause ST segment depression (31). However, the use of a catheter in the cubital vein may be a relatively insensitive way to characterize myocardial potassium delivery compared with arterial or arteriovenous blood sampling over a specified group of exercising skeletal muscles, for example, in the leg. Since the exercise in the present study was carried out on a bicycle, only a minor part of the work was done by the arm muscles. Thus, the arm muscles may extract rather than release potassium so that the concentration in the cubital vein may be underestimated compared with the central vessels.

Conclusions and implications.   So far, we have demonstrated that potassium metabolism during exercise is altered in patients with syndrome X. These findings may account for the high prevalence of generalized fatigue in the skeletal muscles (8), because excessive potassium efflux from skeletal muscle reduces the potassium gradient between the intra- and extracellular compartments and impairs action potential transmission and consequently tension development (32). Potassium acts as a mediator of cardiac pain per se (33,34) and in combination with other chemical mediators such as adenosine (35). Whether the abnormal potassium handling in patients with syndrome X also involves cardiac muscle, causing localized interstitial hyperkalemia, cannot be determined from the present study. In the absence of any demonstrable perfusion abnormality, the uptake and washout of the potassium analog thallium-201 is reduced in patients with syndrome X (36). This may be a result of abnormal myocardial potassium handling.


   Acknowledgments
 
We thank Ms. Eva Sparrewath, Ms. Bente Jacobsen, Ms. Birthe Baumgarten and the staff of the Department of Biochemical Chemistry, Skejby Hospital for skillful laboratory assistance.


   Footnotes
 
This study was supported by a grant from the Danish Heart Foundation.


   References
Top
 Abstract
 Methods
 Results
 Discussion
 References
 

  1. Camici PG, Marraccini P, Lorenzoni R, et al. Coronary hemodynamics and myocardial metabolism in patients with syndrome X: response to pacing stress. J Am Coll Cardiol. 1991;17:1461–1470[Abstract]
  2. Bøtker HE, Sonne HS, Bagger JP, Nielsen TT. Impact of impaired coronary flow reserve and insulin resistance on myocardial energy metabolism in patients with syndrome X. Am J Cardiol. 1997;79:1615–1622[CrossRef][Medline]
  3. Poole-Wilson PA. Potassium and the heart. Clin Endocrinol Metab. 1984;13:249–268[CrossRef][Medline]
  4. Webb SC, Poole-Wilson PA. Potassium exchange in the human heart during atrial pacing and myocardial ischaemia. Br Heart J. 1986;55:554–559[Abstract/Free Full Text]
  5. 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[Abstract/Free Full Text]
  6. Bøtker HE, Sonne HS, Sørensen KE. Frequency of systemic microvascular dysfunction in syndrome X and variant angina. Am J Cardiol. 1996;78:182–186[Medline]
  7. Opherk D, Schuler G, Wetterauer K, Manthey J, Schwarz F, Kubler W. Four-year follow-up study in patients with angina pectoris and normal coronary arteriograms ("syndrome X"). Circulation. 1989;80:1610–1616[Abstract/Free Full Text]
  8. Bass C, Wade C, Hand D, Jackson G. Angina with normal and near-normal coronary arteriograms: clinical and psycho-social state 12 months after angiography. BMJ. 1983;ii:1505–1508
  9. strand I. Aerobic work capacity of men and women with special reference to age. Acta Physiol Scand. 1960;169(Suppl):49–92
  10. Myers J, Froelicher VF. Exercise testing. Procedures and implementation. Cardiol Clin. 1993;11:199–213[Medline]
  11. strand P, Rodahl K. Textbook of Work Physiology. New York: McGraw-Hill; 1970. p. 280
  12. Eriksson B, Persson B. Determination of catecholamines in rat heart tissue and plasma samples by liquid chromatography with electrochemical detection. J Chromotogr. 1982;228:143–154
  13. Hohorst HJ. L-(+)-Lactate, determination with lactate dehydrogenase and DPN. Bergmeyer HU. Methods of Enzymatic Analysis. New York: Academic Press; 1963. p. 266–270
  14. Clausen T. Regulation of active Na+,K+ transport in skeletal muscle. Physiol Rev. 1986;66:542–580[Free Full Text]
  15. Holdright DR, Rosano GMC, Sarrel PM, Poole-Wilson PA. The ST segment—the herald of ischaemia, the siren of misdiagnosis, or syndrome X? Int J Cardiol. 1992;35:293–301[CrossRef][Medline]
  16. Lindinger MI. Potassium regulation during exercise and recovery in humans: implications for skeletal and cardiac muscle. J Mol Cell Cardiol. 1995;27:1011–1022[CrossRef][Medline]
  17. Castellino P, Simonson DC, DeFronzo RA. Adrenergic modulation of potassium metabolism during exercise in normal and diabetic humans. Am J Physiol. 1987;252:E68–E76
  18. Barlow CW, Qayyum MS, Davey PP, Conway J, Paterson DJ, Robbins PA. Effect of training on exercise-induced hyperkalemia in chronic heart failure. Relation with ventilation and catecholamines. Circulation. 1994;89:1144–1152[Abstract/Free Full Text]
  19. McKenna MJ. Effects of training on potassium homeostasis during exercise. J Mol Cell Cardiol. 1995;27:941–949[CrossRef][Medline]
  20. Coplan NL, Gleim GW, Nicholas JA. Exercise-related changes in serum catecholamines and potassium: effect of sustained exercise above and below lactate threshold. Am Heart J. 1989;117:1070–1075[CrossRef][Medline]
  21. Romeo F, Gaspardone A, Ciavolella M, Gioffré P, Reale A. Verapamil versus acebutolol for syndrome X. Am J Cardiol. 1988;62:312–313[CrossRef][Medline]
  22. Rosano GMC, Ponikowski P, Adamopopoulos S, et al. Abnormal autonomic control of the cardiovascular system in syndrome X. Am J Cardiol. 1994;73:1174–1179[CrossRef][Medline]
  23. Frøbert O, Mølgaard H, Bøtker HE, Bagger JP. Autonomic balance in patients with angina and a normal coronary angiogram. Eur Heart J. 1995;16:1356–1360[Abstract/Free Full Text]
  24. Todd EP, Vick RL. Kalemotropic effect of epinephrine: analysis with adrenergic agonists and antagonists. Am J Physiol. 1971;120:1963–1969
  25. Williams ME, Rosa RM, Silva P, Brown RS, Epstein FH. Impairment of extrarenal potassium disposal by a-adrenergic stimulation. N Engl J Med. 1984;311:145–149[Abstract]
  26. Camici PG, Marraccini P, Gistri R, Salvadori PA, Sorace O, L’Abbate A. Adrenergically mediated coronary vasoconstriction in patients with syndrome X. Cardiovasc Drugs Ther. 1994;8:221–226[CrossRef][Medline]
  27. Williams ME, Gervino EV, Rosa RM, Landsberg L, Young JB, Epstein FH. Catecholamine modulation of rapid potassium shifts during exercise. N Engl J Med. 1985;312:823–827[Abstract]
  28. Bøtker HE, Møller N, Schmitz O, Bagger JP, Nielsen TT. Myocardial insulin resistance in patients with syndrome X. J Clin Invest. 1997;100:1919–1927[Medline]
  29. Eckel J, Reinauer H. Insulin action on cardiac glucose transport. Studies on the role of the Na+/K+ pump. Biochim Biophys Acta. 1983;736:119–124[Medline]
  30. Ferrannini E, Taddei S, Santoro D, et al. Independent stimulation of glucose metabolism and Na-K exchange by insulin in the human forearm. Am J Physiol. 1988;255:E953–E958
  31. Gettes LS. Electrolyte abnormalities underlying lethal and ventricular arrhythmias. Circulation. 1992;85:I-70–I-77
  32. Sjøgaard G. Water and electrolyte fluxes during exercise and their relation to muscle fatigue. Acta Physiol Scand. 1986;126:129–136
  33. Webb SC, Canepa-Anson R, Rickards AF, Poole-Wilson PA. High potassium concentration in a parenteral preparation of glyceryl trinitrate. Need for caution if given by intracoronary injection. Br Heart J. 1983;50:395–396[Abstract/Free Full Text]
  34. Meller ST, Gebhart GF. A critical review of the afferent pathways and the potential chemical mediators involved in cardiac pain. Neuroscience. 1992;48:501–524[CrossRef][Medline]
  35. Sylvén C. Neurophysiological aspects of angina pectoris. Z Kardiol. 1997;86:95–105[CrossRef][Medline]
  36. Rosano GM, Peters NS, Kaski JC, et al. Abnormal uptake and washout of thallium-201 in patients with syndrome X and normal-appearing scans. Am J Cardiol. 1995;75:400–402[CrossRef][Medline]



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