JUNE
The American
Journal
1976
of CARDIOLOGY@ VOLUME
37
NUMBER 7
CLINICAL
STUDIES
Myocardial Bridging and Milking Effect of the Left Anterior Descending Coronary Artery: Normal Variant or Obstruction?
JACQUES MARTIAL ROBERT IHOR
NOBLE, MD G BOURASSA, PETITCLERC,
DYRDA,
MD,
MD,
FACC
MD
FACC
Montreal, Quebec, Canada
From the Montreal Heart lnsthte and Departments of Medlctne and Radiology, Unlverslty of Montreal Medical School, Montreal, Quebec, Canada This work was supported by the Jean-Louls Levesque Foundatton, Montreal, Quebec, Canada Manuscript accepted November 26, 1975 Address for reprints Martial G Bourassa, MD, Montreal Heart Institute. 5000 East, Belanger St , Montreal, Quebec HlT lC8, Canada
Of 5,250 patients undergoing coronary arteriography over a 5 year period, 27 (0.51 percent) had an intramyocardial segment of the left anterior descending coronary artery producing a milking effect or constriction of the artery during systole. Of these, 11 patients with otherwise normal coronary arteries were studied. Hemodynamic data, coronary sinus blood flow and myocardial lactate extraction were measured during atrial pacing at rates of 120 and 150 beats/min and during a 60 watt supine ergocycle exercise test. The degree of narrowing of the left anterior descending coronary artery during systole was graded 3 (greater than 75 percent), 5 patients; 2 (50 to 75 percent), 4 patients; and 1 (less than 50 percent), 2 patients. Four patients with a grade 3 milking effect had S-T depression in the electrocardiogram indicating anterior wall ischemia and lactate production during pacing at 149 f 2 (mean f standard error of the mean) beats/min. Three patients had severe angina during pacing. Two patients with a grade 2 milking effect had angina-like chest pain and electrocardiographic changes during pacing at 150 beats/min. However, lactate extraction was unchanged during pacing. Two patients with a grade 1 milking effect had no angina and no electrocardiographic or metabolic abnormalities. Coronary sinus blood flow increased significantly with pacing and ergocycle exercise in all patients (rest 116 f 6 ml/min; pacing at 150 beats/min 219 f 27 ml/min; ergocycle exercise 251 f 17 ml/min) (P
A milking effect or transient narrowmg of an artery on selectrve coronary arterlography was first described m 1960 by Portsmann and 1wrg.l This arterlographlc appearance is very characterrstlc and corresponds to a systolic construction of a segment of the left anterior descendmg coronary artery that is embedded m the myocardmm for a variable distance This segment is squeezed by contraction of the surrounding muscle The constriction disappears durmg diastole.2
June 1976
The American Journal of CARDIOLOGY
Volume
37
993
MILKING EFFECT OF LEFT ANTERIOR DESCENDING ARTERY-NOBLE
ET AL
This radiologic anomaly was found in a group of patients referred to our institution for assessment of chest pain and selective coronary arteriography. The pathophysiologic significance of angina-like chest pain and milking effect with myocardial bridging of one coronary artery is still unknown. Recently, a young man with a history of repetitive chest pain was treated surgically, using a periarterial muscle resection to decompress the squeezed coronary artery. Postoperative follow-up studies seemed to demonstrate relief of chest pain.3 The purpose of this study was to assess whether, at rest or during pacing-induced tachycardia and supine bicycle ergometer exercise, this angiographic anomaly presents a clinical pattern compatible with myocardial ischemia. The presence or absence of hemodynamic and metabolic consequences of a milking effect on the myocardium may provide physiologic criteria for or against a surgical approach in patients with typical or atypical chest pain.
of this evidence and a similar unpublished experience at this center, coronary arteriography was not repeated in our patients before the present investigation. During the follow-up period, all patients remained symptomatic and experienced little change in their clinical status. The coronary nrteriograms were reviewed by at least two experienced observers, and the degree of narrowing of the left anterior descending coronary artery during systole (milking effect) was assessed as grade 3 (greater than 75 percent narrowing) (Fig. 1); grade 2 (50 to 75 percent narrowing); or grade 1 (less than 50 percent narrowing). Five patients had a grade 3, four a grade 2 and two a grade 1 milking effect (Table I). The left ventriculograms were also reviewed, and in three patients, of whom one had a grade 3 and two a grade 2 milking effect, a mild to moderate diffuse hypertrophy of the left ventricle was believed to be present. One patient (Case 3) with a grade 3 milking effect had mild hypertrophic subaortic stenosis. The hemodynamic data of this patient disclosed no intraventricular pressure gradient at rest and a 30 mm Hg intraventricular gradient during isoproterenol stimulation (Table I).
cause
Methods Clinical Patient Selection Of 5,250 patients undergoing coronary arteriography at the Montreal Heart Institute, 27 (0.51 percent) were found to have an intramural segment of the left anterior descending coronary artery producing a milking effect. In this group of patients (mean age 48 years; range 28 to 59 years), 17 had otherwise normal coronary arteriograms and 10 had coronary artery disease. After exclusion of 10 patients with coronary atherosclerosis, 2 with valvular disease, 3 with cardiomyopathy with left ventricular failure or severe arrhythmias and 1 patient who refused study, 11 patients (mean age 46 years; range 31 to 59 years) with a milking effect and otherwise normal coronary arteriograms were selected for hemodynamic and metabolic study. Coronary arteriography and left ventriculography using previously described techniques* were performed 1 month to 4 years (average 22 months) before study. Several recent reports have shown that in adult patients with initially normal coronary arteriograms evidence of coronary artery disease does not develop during a 4 to 5 year follow-up period.5x6 Be-
Information
All patients had a history of repetitive chest pain and were considered on admission to have chronic coronary heart disease severe enough to justify coronary arteriography. The chest pain was assessed as (1) typical angina pectoris (substernal pressure or pain of brief duration, occurring during exertion and relieved by rest, six patients); or (2) atypical angina (chest pain of longer duration and occurring mainly at rest, five patients) (Table I). Investigative
Procedure
After an overnight fast and intramuscular premeditation with meperidine, 50 mg, and promethazine, 25 mg, 11 patients underwent cardiac catheterization. Informed consent was obtained for the procedure. A 100 cm no. i’F, Ganz thermodilution catheter (Wilton Webster Co., Altadena, Calif.) was inserted from a right antecubital vein into the main coronary sinus. The external thermistor or distal pacing electrode of the Ganz catheter was positioned just inside the coronary sinus ostium to obtain the measurement of total coronary sinus blood flow and to avoid hyperselectivity of the catheter
FIGURE 1. Case 3. Cineangiograms obtained in the lateral position in a patient with a grade 3 milking effect. A, during systole, showing severe (more than 80 percent) systolic constriction of the proximal third of the leff anterior descending coronary artery (arrows). B, during diastole. The constriction has disappeared completely, and the left anterior descending coronary artery appears normal.
994
June 1976
The American
Journal of CARDIOLOGY
Volume
37
MILKING EFFECT OF LEFT ANTERIOR DESCENDING ARTERY-NOBLE
trp m the great cardiac vem Location of the catheter was determined and filmed m two positions (anteroposterlor and 30’ right anterior obhque) during a small hand mJectlon of contrast material A no 18 gauge polyethylene catheter was mtraduced percutaneously mto the right radial artery Catheters were connected to Statham P23Db transducers adjusted so that zero pressure was at the level of the mid-chest A 12 lead electrocardiogram was recorded every 30 seconds The protocol was duded into two stages Stage I was not carried out until at least 10 mmutes after catheter manipulations The following measurements were always taken m the same sequence pressure recordmgs, coronary smus blood flow measurement and simultaneous blood samples from the radial artery and mid-coronary sinus Stage I was dlvlded mto three steps (1) rest, (2) atrlal pacing at 119 f 2 beats/mm (lZO/min) from the 1st to the 7th minutes with all measurements taken from the 4th to the 7th minutes, (3) atria1 pacing at 149 f 2 beats/mm (150/mm) from the 7th to the 14th minutes with all measurements taken from the 11th to the 14th minutes After a 15 mmute Interval, stage II was mrtiated wrth expired gas collection, pressure recordings, coronary sinus blood flow measurement, arterial and venous blood samples, cardiac output measurement This stage consisted of two steps: (1) rest, and (2) a 60 watt exercise test on a bicycle ergometer m the supme position for 7 minutes Each complete set of measurements was obtained m less than 3 minutes.
mixture of blood and injectate (“C), and 1 19 is a constant derived from the density and specific heat of the salme solution and blood Blood samples were obtained simultaneously from the radial artery and the coronary sinus and immediately analyzed for pH, and partial pressure of oxygen (PO2) and carbon dioxide (PCOJ by a Micro-Astrup analyzer Hemoglobm saturation was obtained from the oxyhemoglobin dlssociatlon curve with correction for pH and temperature, as described by Severmghaus 8 Samples of arterial and coronary emus blood were also taken for determmations of lactate concentration by the enzymatic method of Hochella and Wemhouse g The following calculatlons’e were made Left ventricular oxygen and lactate extraction (g/o)
Milking
Effect
of Left Anterior
AngIna-llke
=
Character
58M 31 F 42F 48F 52F 6 7 8 9 10 11
Case no
SVR = (MAP x SO)/CO
Pacing at 150Imln
TypIcal TypIcal Typical Atyptcal Atyplcal
3 1 :
Severe Severe Severe No No
50F 54M 59M 34M
Typical TypIcal TypIcal Atyplcal
3 l/2 i!i 2
Mlld Mild No No
50M 35F
Atyplcal AtypIcal
1 l/2 I
No No
had hypertrophlc
Artery.
Clmical,
where MAP indicates mean arterial pressure m mm Hg, CO is cardiac output m liters/mm, and 80 ISthe conversion factor to express resistance m absolute units
Anglographic
2
subaortlc
stenosis
and Metabolic
Abnormalities
m 11 Cases
Electrocardiogram
During Stress
Duration (yr)
“This patlent
mean aortlc pressure (mm Hg) coronary sinus blood flow (ml/mm)
Systemic hemodynamic? and derived variables: Pressures were amphfred and recorded at paper speeds of 25 and 100 mm/set on a multichannel photographic recorder Pressure readings and calculations of the systolic eJection time were always the mean of 10 beats Cardiac output was measured after rapid mJectlon of 5 mg of mdocyanme green dye mto the coronary sinus, followed immediately by a saline flush Arterial blood was withdrawn by a Harvard mfuslon pump at a rate of 20 ml/mm through a cuvette dye densitometer. Computation of the cardiac output was performed with the use of the Willlams formula l1 Systemrc vascular resistance (SVR in dynes set cmp5) was calculated as follows
Chest Paln
Before Study Age (yr) & Sex
(ml/mm)
Coronary resistance (mm Hg/ml per mm)
1.19
Descendmg
oxygen or lactate
= [arterial - coronary sinus 0s content (ml/100 ml)] X coronary sinus blood flow (ml/mm) X 10-s,
where Fi represents the volume of inJectate (ml/min), Tb, Ti and Tm are, respectively, temperatures of blood, inJectate and
I
arterial
Left ventricular oxygen consumption
Coronary hemodynamics and metabolism: Coronary smus blood flow was measured by the thermodilutlon method 7 A physiologic sahne solutron at 22 to 25O C was injected into the coronary sinus, using a calibrated Harvard pump and twm syringes of 20 ml, at a constant rate of about 38 8 ml/mm for 20 to 30 seconds. Estimation of total coronary blood flow by this sample method has been found highly reproducible m our laboratory Varrations between two successive measurements have not exceeded 5 percent Coronary sinus blood flow (CSBF m ml/mm) was calculated usmg the following formula7:
TABLE
arterial - coronary sinus
=
Measurements
CSBF = Fr <,‘,“_;;,
ET AL
Supine Exercise
Resting ST-T Abnormal ItIes
lschemlc Changes Supine Exercise
Pacing at 150Imln
Grade 3 Mllklng Effect Moderate Yes V&-V, Yes Moderate V,-V,.D, No No V,-V, No No V, No No No Grade 2 Mtlktng Effect No Yes V,-V, No Yes V, No Yes No No No No Grade 1 Mllklng Effect No No No No No No
No
Left Ventrlculogram
Contractlon
Hypertroohv
Abnormal Lactate Extractton During Pacing at 150lmln Yes(O%)
Normal Normal
No Yes Yes* No No
v,-v, v,-v, No No
Normal Normal Increased Increased
No No Yes Yes
No(+14%) No(+8%) No(+23%) Not+1 5%)
No No
Normal Normal
No No
Not+31 %) No(+23%)
V,.V&,
No V4 No
Normal Normal
Increased
Yest-45%) Yes(-42%) Yesl-35%) No(+21%)
See text
June 1976
The American
Journal
of CARDIOLOGY
Volume
37
995
MILKING EFFECT OF LEFT ANTERIOR DESCENDING ARTERY-NOBLE
Tenston-tsme mdex measured as follows
(TTI
ET AL
m mm Hg/sec per mm) was
Results There
Mean systoh eJectLon rate (MSER m ml/set per m2) was calculated as follows MSER = SI/SEP where SI ISthe stroke mdex m ml/beat per m2 and SEP is the systolic election period m set/beat At rest and during supme ergometer exercise, expired gas was collected m a Tlssot spirometer m order to measure total body oxygen consumption (VOs m ml/mm) Statrstzcal analysts was performed with the use of a paired Student’s t test Values at rest were compared with values obtained during atria1 pacing at 120 and 150/mm and during exercise testing All calculations were accomplished with use of an electronic calculator usmg the same program (Hew-
Systemic
of Systemic Hemodynamlc _____
Heart rate (beats/mln) Arterial pressures (mm Hg) Systolic Dlastollc Mean Cardiac Index (Ilterslmin per m.“) Systemic vascular resistance (dynes set cm”) Tenston-time Index (mm Hg/sec per mln) Mean systolic electIon rate (ml/set per mm) Oxygen consumption (ml/mln)
II)
error of the mean)
Pacing
Exercise Testing
120/mm
7% + 6
127 +_5 66 ? 3 87 + 3
150/mm
Control
Supine Exercise
87 t 6
119+2*
149+_2*
128+4NS 75 + 2+ 92 k 3 NS
123?6NS 77 t 2+ 90 +_3 NS
126~4~
162? 5” 78 + 2+ 105 + 3”
130t5 72 t 3 91 f 3 35o-to3
+ P values derived from Student’s
palred t test lndlcate
difference
from control
values
* = P < 0 001,
640+04”
1340
+_ 121
2693
i- 200
835 ? 80’ 4180
? 235”
151 f 15
217 ? 18”
216 * 14
891 * 55”
t =P
< 0 05, NS = not sqnlflcant
III Hemodynamlcs
and Myocardlal ___--
Metabolism
(mean values + standard Atrlal
Control Coronary sinus blood flow (ml/min) Coronary reststance (mm Hg/ml per mln) LV oxygen extractlon (%I LV oxygen consumption (ml/mln) LV lactate extractnon (%) Grade 3 mllklng effect (no = 5) Grade 2 mllklng effect (no = 4) Grade 1 mllklng effect (no = 2)
l+S P values derived from Student’s slgnlflcant LV = left ventricular
996
(Table
__-
Control
Coronary
Hemodynamics
Data m 11 Cases (mean values + standard Atrlal
TABLE
pa-
II
Summary
l
among the individual
Durug atrzal pacq at heart rates of 119 f 2 and 149 f 2 beats/mm (mean f standard error of the mean), systolic and mean arterial pressures were unchanged and dlastohc arterial pressure increased (P
lett-Packard calculator 9830A with dlgltrzer)
TABLE
was some varlatron
tients m the systemic and coronary hemodynamlc response to atria1 pacing and to brcycle ergometer exercrse. However, the varratlon was not related to the degree of milking effect of the left anterior descending coronary artery observed at coronary arteriography. The hemodynamic results of all three groups (grades 1, 2 and 3 milking effect) were comparable and will be discussed together
TTI = (HR) x (SEP) x (MSAP)
June 1976
1202
7
0 75 * 0 05
15+6
Pacing
Exercise Testing
120/mln
150lmin
172 + 12”
218 +_25+
0 56 + 0 043
046+006+
57 ? 5 NS
56+5NS
61 -f 5 125r16
error of the mean) I__-
163+
-18
17*
205?3*
-21
+ 17
15*
19 * 5
23 +_4
27 ? 4
The Amencan Journal of CARDIOLOGY
Volume 37
073+004 60 ? 6
+9
191t9
from control
132 + 10
135+18
15 + 8
palred t test lndlcate difference
Control
3
values
* = P < 0 01. ~=P
Supine Exercise 240 i 19+ 046+
03+
59i6NS 236228”
MILKING
systolic (P
and Myocardial
Metabolism
Mean coronary sinus blood flow increased from 120 f 7 ml/min at rest to 172 f 12 (P
ml/m
360
Mean tSEh4 / 9
MILKING grads grads grade
EFFECT
OF LEFT
ANTERIOR
DESCENDING
ARTERY-NOBLE
ET AL
(Fig 4) In five patients with a’grade 3 milking effect, mean lactate extraction was 15 f 6 percent at rest and shifted to lactate production during pacing: -18 f 17 percent at a pacing rate of 120/mm and -21 f 9 percent at a rate of 150/min. In four patients with a grade 2 milking effect and in two patients with grade 1 effect, mean lactate extraction was unchanged during pacing (Fig. 4). Four of five patients with a grade 3 milking effect had lactate production or absence of extraction at a pacing rate of 150/min; all patients with a grade 2 or grade 1 milking effect had a normal lactate extraction at this pacing rate (Fig 4) Clinical Correlates
(Table I)
Chest pain: Three of five patients with a grade 3 milking effect had severe angina-like chest pain at both pacing rates. The pain persisted while all determinations were being obtained during pacing (approximately 3 minutes) and was immediately relieved after discontinuation of pacing. Two of these five patients also had angina-like chest pain during exercise that persisted until the exercise was discontmued. Two of four patients with a grade 2 milking effect had chest pam at a pacing rate of 150/min but no chest pain during exercise None of the two patients with a grade 1 milking effect manifested either pacing-induced or exercise-induced chest pain.
EFFECT 3 l 2 m 1 A
ml/mm 40
320
MILKING EFFECT grade 3 . grade 2 . grade 1 A
Mean +SEM
35
160
120
60
, REST
p
,
I
PACING 15O/mm
REST
p
,
EXERCISE
I
REST
FIGURE 2. CoronarySIWJS blood flow at rest, dunng atnal pacing at 120 and 150/min (10 cases) and during supine bicycle ergometer exercise (9 cases) Coronary slnus blood flow increases In all three groups (grades 1, 2 and 3 mllklng effect), and the average increase In coronary flow IS comparable during atrial pacing at 150/mln and during supine exercise Mean f SEM = mean value i standard error of the mean value, p = probability
PACING 120/mm
PACING lSO/mm
REST
p
, EXERCISE
FIGURE 3. Left ventricular oxygen consumption at rest, during atria1 pacing at 120 and 150/mln (10 cases) and dunng supine bicycle ergometer exercise (9 cases) Left ventricular oxygen consumption Increases to a comparable level during atnal pacing at 150/m1n and during supine exercise Mean f SEM = mean value f standard error of the mean value
June 1976
The American Journal of CARDIOLOGY
Volume 37
997
MILKING EFFECT OF LEFT ANTERIOR DESCENDING ARTERY-NOBLE
ET AL
REST PACING 120/mm
DI
02
D?
PACING
DI
FIGURE 4 Left ventrrcular lactate extractron durrng atrral pacrng at 120 and 150/mm (11 cases) Lactate extractron IS closely related to the degree of mrlkrng effect Four of five patrents with a grade 3 mrlkrng effect have a lactate production or absence of extractron at a pacing rate of 150/mm Patients wrth a grade 2 or grade 1 mrlkrng effect have a normal lactate extraction at the same pacrng rate (150/mm) Mean = mean value
S-T changes: Four of five patients with a grade 3 milking effect had “ischemic” ST-T segment changes in the precordial leads of the electrocardiogram at the higher pacing rate (Fig. 5) Two of these 5 patients showed similar changes durmg supine exercise. Two of four patients with a grade 2 milking effect also demonstrated “ischemic” ST-T segment changes (1 mm or more) in the precordial leads at the higher pacing rate and during supine exercise Of the four patients with a grade 3 milking effect, chest pain or ST-T ischemic changes, or both, and abnormal lactate metabolism during stress, one had mild diffuse left ventricular hypertrophy and one had a mild hypertrophic subaortic stenosis demonstrated by left ventriculography Both patients with a grade 2 milking effect, chest pain and ST-T changes and normal lactate metabolism during stress had a normal left ventriculogram. Discussion The mtramyocardial course of a segment of the left anterior descending coronary artery was first described in 1922 by Cramicianui2 and is well known to pathologists. is A 23 percent incidence rate of this variation was observed at autopsy by Geiringer.13 The cardiac surgeon is sometimes confronted with the technical problem of an intramyocardial left anterior descending coronary
996
June 1976
The American Journal of CARDIOLOGY
Volume 37
D2
&I
AVR
AVL
AVF
150/min AVR
AVL
AVF
FIGURE 5 Case 3 Electrocardrogram at rest and during atria1 pacing at 150/mm Top, the resting electrocardrogram shows normal S-T segments and T waves Bottom, during atria1 pacing at 150/mm, there IS srgnrfrcant S-T segment depression in leads Vq, Vs and Vs
artery when this vessel is dissected for an aortocoronary bypass In 1960, Portsmann and Iwigi reported the first radiologic description of transient occlusion m a segment of the left anterior descending coronary artery during systole In 1968, Amplatz and Anderson2 emphasized the transient nature of coronary arterial narrowing and the importance of differentiating myocardial bridging from fixed atherosclerotic stenosis As yet, no cineangiographic and anatomic correlation has been carried out The origin of this arterial anomaly is probably congenital in light of the intramural location of the left anterior descending artery during embryonic life l3 The delayed appearance of symptoms in these patients remains unexplained, although an increase in systolic wall tension and the acquisition of the milking effect might be secondary to gradual growth of the heart muscle and to left ventricular hypertrophy The association of unexplained diffuse left ventricular hypertrophy m 3 of the 11 patients and of true hypertrophic cardiomyopathy in 1, as demonstrated at left ventriculography, is probably significant and is currently under study in our larger series of 27 patients. It appears to be present m about one fourth of patients with myocardial bridging.
MILKING EFFECT OF LEFT ANTERIOR DESCENDING ARTERY-NOBLE ET AL
Mechanism of ischemic syndrome: Our investlgatlon strongly suggests that patients with a grade 3 milking effect, corresponding to more than 75 percent narrowing of the left anterior descendmg coronary artery during systole, can experience severe myocardial ischemla, especially during rapid heart rates. Although the coronary narrowing occurs selectively during systole, the pathophyslologic mechanism of this ischemlc syndrome, without coronary atherosclerotic disease, is probably related to a shortenmg of the diastohc fillmg time when the heart rate is increased above a given level. The association of a significant coronary narrowing during systole (75 percent or more) and a very short diastolic time period produce a hemodynamlc condition functionally similar to an atherosclerotic obstruction. Diastolic relaxation of the coronary artery may also be decreased, a possibility that could be verified by injection of contrast material into the left anterior descending coronary artery during atria1 pacing. In patients with a grade 3 milking effect coronary sinus blood flow during pacing and during supine exercise was not significantly different from that in patients with a less severe milking effect. Moreover, coronary blood flow showed no tendency to decrease during
acute ischemia, and no other significant hemodynamlc abnormality was demonstrated. It is likely that the obstruction of a single coronary artery changes regional blood flow but is msufficient to unbalance the total myocardlal perfusion of the left ventricle. Clinical implication: The heart rates of 150 beats/ mm employed in our protocol are not representative of normal daily activities Our observations suggest that at heart rates of 120 beats/min or less, untoward effects of ischemia are less likely to occur. Under these conditions, medical or surgical treatment of these patients would not be systematically indicated. Advising the patient to avoid strenuous exercise should be sufficient to prevent episodes of pain Propranolol could attenuate the effects of increased heart rate and contractility m these patients. Finally, one cannot exclude the possibility that surgical dislodgment of the embedded segment of the left anterior descending coronary artery or an aortocoronary bypass would be useful in some subjects who are severely incapacitated or obliged to perform heavy work. This theoretical mdication for surgery might occur in rare cases, and the surgical risk would have to be weighed against the unknown prognosis of this anomaly.
References 1 Porismann W, lwig J: Dre lntramuraleKoronarre rm Angtogramm Fortschr Rontgenstr 92 129-132, 1960 2 Amplatz K, Anderson R: Angrographrc appearance of myocardral bridging of the coronary artery Invest Radio1 3 213-215, 1968 3 Binet JP, Piot C, Planche C, et al: “Pont myocardrque” compnmant I’a&re rnterventncularre anteneure a propos d’un cas opere avec succes Arch Mal Coeur 68 87-90, 1975 4 Bourasaa MG, Lesp(?rance J, Campeau L, et al: Selective coronary angrography using a percutaneous femoral technique Can Med Assoc J 102 170-173, 1970 5 Gensfni GG, Esente P, Kelly A: Natural history of coronary disease in patients with and without coronary bypass graft surgery Crrculatron 49, 50 Suppl II 11-98-11-102, 1974 6 Bruschke AVG, Proudfit WL, Sones FM Jr: Clrnrcal course of pabents with normal and slightly or moderately abnormal coronary arterrograms A follow-up study on 500 patients Circulation 47 936-945, 1973 7 Ganz W, Tamura K, Marcus HS, et al: Measurement of coronary
8
9 10
11
12
13
June 1976
srnus blood flow by conbnuous thermodrlutron In man Crrculabon 44 181-195, 1971 Severinghaus JW: Oxyhemoglobin drssocratron curve correction for temperature and pH variation in human blood J Appl Physrol 12 485-489, 1958 Hochella NJ, Weinhouse S: Automated lactrc acid determtnatron in serum and tissue extracts Anal Blochem 10 304-308, 1965 Gorlin Ft. Measurement of coronary flow in health and disease In, Modern Trends In Cardiology (Jones AM ed) New York, Paul B Hoeber, 1960, p 191 Willlams JCP, O’Donovan TPB, Wood EH: A method for calculation of areas under mdrcatordrlutroncurves J Appl Phys10121 695-699, 1966 Crainicianu A: Anatomrsche Studlen you ber bre coronararterren und exterrnentelle Untersuchungen uber rhre Durchgangrgkert Vrrchows Arch Pathol Anat 238 1-8, 1922 Geiringer E: The mural coronary Am Heart J 41 359-368, 1951
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Volume 37
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