Cerebral Arteriovenous Malformation as a Cause of Cardiac Hypertrophy in Adults. Masatoshi FUJISHIMA, M.D., Kenjiro TANAKA, M.D., and Teruo OMAE, M.D.
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1 Cerebral Arteriovenous Malformation as a Cause of Cardiac Hypertrophy in Adults Masatoshi FUJISHIMA, M.D., Kenjiro TANAKA, M.D., and Teruo OMAE, M.D. SUMMARY Seventeen adult patients with cerebral arteriovenous malformation were studied on cardiac effects of this disease. Of all 17 patients tested, the electrocardiogram revealed left ventricular hypertrophy in 5, sinus bradycardia in 4, WPW syndrome in one, and no abnormality in 7 others. There were 3 patients having a slight increase in the cardiothoracic ratio over 51%, and 14 having normal heart size determined from the chest X-ray taken. Of all 11 patients, in whom brain circulation was measured by the intravenous RISA technique, cranial blood flow (CBF) increased significantly in 5, remained within normal value in 4, and slightly decreased in 2 patients. Left ventricular hypertrophy on ECG was observed in 3 of 5 patients with a high CBF, but in none from the patients with normal or subnormal CBF, suggesting that the occurrence of ventricular hypertrophy was highly related with an increased CBF. The relationship between cerebral arteriovenous malformation and cardiac changes is discussed. Additional Indexing Words: Cranial blood flow Brain transit time Left ventricular hypertrophy Cardiothoracic ratio ERIPHERAL arteriovenous fistulas such as the femoral, the brachial and the carotid have been reported to cause elevation of cardiac output, changes in systemic hemodynamics, and increase in cardiac size.1)-3) Furthermore, it is not uncommon to be cause of heart failure in femoral arteriovenous fistulas.4) Intracranial arteriovenous malformation (AVM), however, has been observed to cause congestive heart failure in newborn infants,5)-8) but it has not been reported in adults. In the present study, cardiac enlargement or left ventricular hypertrophy (LVH) was demonstrated in adult patients with intracranial AVM. METHODS The patients were 14 males and 3 females with an average age of 35 years and From the Second Department of Internal Medicine, Faculty of Medicine, Kyushu University, 1276 Katakasu, Fukuoka 812, Japan. Received for publication August 18,
2 472 FUJISHIMA, TANAKA, AND OMAE Jap. Heart J. N ovember, years respectively. Twelve of all 17 patients were diagnosed as subarachnoid hemorrhage, and 5 others as Jacksonian epilepsy. No patient had a history of heart diseases, hypertension, or renal diseases. Cranial blood flow (CBF), brain transit time (TT), and arm-to-brain circulation time (ABCT) were measured in 11 patients by the external counting method of the intravenously injected RISA.9) All patients underwent complete neurological examinations and had routine laboratory tests, electrocardiograms (ECG), chest X-rays and bilateral carotid angiograms. None of patients having cerebral "Moyamoya" disease, or fistula between the extracranial artery and the intracranial vein was included in this series. RESULTS Clinical Findings: Either systolic or diastolic blood pressure was normal in all but one having a mild hypotension (Table I). The average blood pressure of all patients was 119mm. Hg systolic, and 65mm. Hg diastolic. Seven had normal ocular fundi, 8 had a mild retinopathy of group 1 by Keith-Wagener's classification, and 2 others had a papilledema. No patient had heart murmur or proteinuria, and 2 had a positive test for syphilis, which had been treated previously. Table I. Clinical Findings in 17 Patients K-W: Keith-Wagener classification, CTR: cardiothoracic ratio, SAH: subarachnoid hemorartery, AVM: arteriovenous malformation
3 Vol.13 No.6 CEREBRAL A-V MALFORMATION 473 The mean hemoglobin value was 14.2Gm./100ml., ranging Gm./100ml. A spinal tap was performed in all but one; 11 having normal cerebrospinal fluid pressure below 200mm. H2O, and 5 having a higher pressure than 200mm. H2O, among which the highest value was 350mm. H2O. There were 3 patients of cardiothoracic ratio (CTR) greater than 51% as determined from the chest X-ray taken, 5 between 46-50%, and the remaining 9 less than 45%. On the cerebral angiograms, there were 12 patients having AVM located in the territories of the middle cerebral artery; in 6 the middle cerebral artery only as a feeding vessel to AVM, in 3 both the middle and the anterior cerebral arteries. Two of all 17 had AVM in the areas of the anterior cerebral artery, and 3 others had of the posterior cerebral artery. The ECG as shown in Table II, revealed normal in 7 patients, sinus bradycardia in 4, LVH in 5, and WPW syndrome in one. A non-specific depression of ST segment was recorded in 2 patients. Electrocardiographic diagnosis of LVH was made on the basis of the voltage criteria described by Mori and his collaborators10),11) SV1+RV5 40mm. (50mm. for adolescent males under age 30), and SV2+RV5+SaVF 45mm. (55mm.). In the latter criteria, a false positivity for LVH was much less frequent and a coincidence with Cerebral Arteriovenous Malformation rhage, MCA: middle cerebral artery, ACA: anterior cerebral artery, PCA: posterior cerebral
4 474 FUJISHIMA, TANAKA, AND OMAE Jap. Heart J. N ovember, 1972 Table II. Electrocardiographic Findings in 17 Patients with Cerebral Arteriovenous Malformation *,** Voltage criteria of Mori, et al., see text, RSR: regular sinus rhythm, LVH: left ventricular hypertrophy, WNL: within normal limits, SB: sinus bradycardia, n: normal, dep, C-L: ST depression in chest and limb leads, J-dep, L: junction typed depression of ST segment in limb leads, neg, C: negative T wave in chest leads, WPW: WPW syndrome with LVH proved at autopsy was higher than that in the former. Eight of the 17 patients took the surgical treatments such as complete extirpation of AVM, or clipping the feeding arteries. Brain Circulation Study: Five of all 11 patients studied had a significant increase in CBF, being greater than 2,000ml./min., 4 had normal CBF, and 2 others a slight decrease in CBF (Table III). The highest CBF was 2,910ml./min., which was double as great as that of normal subjects. The mean CBF was 1,977ml./min. in patients with AVM comparable to that of 1,569ml./min. in the normal subjects aged under, and 1,504ml./min. in those aged over 40 years. In 8 patients, TT was normal but tended to be shorter in the affected * 1) Mori and Kawamata's correction for the Japanese adults of Sokolow -Lyon' criteria for diagnosis of LVH is as follsws: RV5(6)+SV1 40mm. (50mm.), RI+SIII 20mm., RV5 30mm., RV6 23mm., RaVL 11mm., or RaVF 22mm. 2) Mori and Nakagawa's criteria on the basis of total left ventricular potentials is as follows; SV2+RV5+SaVF 45mm. (55mm.), SV2+RV6+ SaVF 40mm. (50mm.), or SV1+RV6+SaVF 35mm. (45mm.). When any one of these items is satisfied, the presence of LVH is sufficiently presumed.
5 Vol.13 No.6 CEREBRAL A-V MALFORMATION 475 Table III. Brain Circulation in 11 Patients with Cerebral Arteriovenous Malformation Measured by Intravenous RISA Technique CBF: cranial blood flow, TT: brain transit time, ABCT: arm-to-brain circulation time, L or R: left or right hemisphere hemisphere than in the contralateral one. In other 3, TT was significantly shorter in both the affected and non-affected hemispheres than that in the control subjects. ABCT, as the sum of the part of systemic and the pulmonary circulation times, was significantly shorter in 2, and normal in 8 of all 10 patients tested. DISCUSSION Five out of the 11 patients tested showed a significant increase in CBF by 33 to 93% from control value. Of these 5 patients, 3 had LVH in their ECGs, one had WPW syndrome, and the remaining one normal ECG. There were no associated conditions such as those of hypertension, arteriosclerosis, severe anemia or renal disease to cause cardiac hypertrophy. In the remaining 6 patients of normal or subnormal CBF, their ECGs showed either normal or sinus bradycardia, but no LVH. These results strongly suggest that LVH found in their ECGs is related to an increase in CBF. On the basis of Mori and his collaborators' criteria for electrocardiographic diagnosis of LVH, a value for SV2+RV5+SaVF 45mm. (55mm. for males under age 30), defined as the summation of left ventricular potential has a almost negligible false positivity and a much higher coincidence with
6 476 FUJISHIMA, TANAKA, AND OMAE Jap. Heart J. N ovember, 1972 the autopsy proved LVH being 70%, than that on the basis of Sokolow-Lyon's original criteria. Besides LVH observed in 5 patients in present series, no other abnormality was found such as a strain pattern of ST segment, or inversion of T waves, which may result from a relative hypoxia of the myocardium. The data may indicate that ECG change in patients with cerebral AVM is much less severe than that frequently observed in cases with hypertensive cardiovascular or cardiac valvular diseases, and might explain why cerebral AVM hardly causes congestive heart failure in the adult. Meanwhile, Cabrera and Monroy12) described that diastolic overloading of left ventricle produces an elevation of R wave and high positive T wave in V5 as well as V6 where the left ventricular potentials are transmitted, whereas in systolic overloading, T wave tends to be flattening or negative with a simultaneous depression of ST segment. Cerebral AVM is the case of diastolic overloading, despite no satisfactory explanation for high T waves. Concerning the brain hemodynamics in cerebral AVM, many investigators observed that CBF increases double as great,13) triple,14) or rarely fourfold15) as that in normal subjects, implying that the estimated cardiac output might simultaneously increase by 750 to 2,250ml./min., or 12 to 35% from normal cardiac output of approximately 6.4L./min. Wallace and his coworkers16) have measured the mean cardiac output in 8 patients with cerebral AVM and in other 8 control patients, being 4.40 and 2.82L./min./M.2 respectively. The average AVM shunt flow in their study was estimated to be 2,804ml./min. on the basis of cardiac output data obtained by a dye-dilution technique, or to be 2,780ml./min. from the systemic arteriovenous difference of oxygen content. It seems unlikely that their estimation of cerebral shunt flow such as these is correct, since the present results show brain transit time being shortened in both the affected and non-affected hemispheres, indicating that CBF increases even in the contralateral hemisphere of cerebral AVM. A similar observation to ours was reported by Lassen and Munck,17) that cerebral blood flow measured by Krypton-85 method was 222ml./100Gm./ min. on the side of AVM, and 108 on the contralateral one before, and 92 and 59ml./100Gm./min. respectively, after a surgical removal of the shunt. Although other studies showed normal appearance times in vessels not feeding the fistula in patients with peripheral arteriovenous anomalies, arm-to-brain circulation time was significantly shortened in some patients of the present study. It is well recognized that arteriovenous fistula of sufficient size such as the femoral may have produced effects on the cardiovascular system. There are increases in blood volume as well as cardiac output primarily due to increase in stroke volume, and may develop congestive heart failure. Although
7 Vol.13 No.6 CEREBRAL A-V MALFORMATION 477 a precise mechanism responsible for the compensatory increases in blood volume and cardiac output has not been fully understood, these cardiac changes are reversible, and the heart size returns to normal after operative removal of the fistula.1) Congestive heart failure has not been uncommon in the newborn or the infant with cerebral AVM. According to the 51 published cases,2) 18 had neonatal congestive heart failure, and 17 of them died within 5 months of age. In the adult cases, however, neither abnormalities of ECG nor changes in cardiac size has been reported. The reason why the cardiovascular effects of cerebral AVM in the adult would be less pronounced than those of the extracranial arteriovenous shunts might be considered as follows; at first, the middle cerebral artery, most frequently implicated as a feeding artery to AVM, is several times smaller in diameter than the peripheral arteries such as the femoral or the brachial.18) Secondly, the intracranial location of AVM higher than heart level might favor a lower shunt flow in the upright posture, and finally, cerebral AVM being enclosed by the skull might retard enlargement of the growth of AVM as well as collateral channels.16) It might be possible, but not fully proved, that in some of the patients with cerebral AVM, congestive heart failure could occur late in life, since a long-lasting hyperkinetic circulatory states19) cause reduction of cardiac reserve,4) and changes in myocardial function resulting in circulatory congestion to develop. REFERENCES 1. Warren, J.V., Nickerson, J.L., and Elkin, D.C.: J. Clin. Invest. 30: 210, Nickerson, J.L., Elkin, D.C., and Warren, J.V.: J. Clin. Invest. 30: 215, Frank, C.W., Wang, H-H., Lammerlant, J., Miller, R., and Weria, R.: J. Clin. Invest. 34: 722, Spurny, O.M. and Pierce, J.A.: Am. Heart J. 61: 21, Hamby, R.I. and Desposito, F.: J. Pediat. 61: 590, Hernandez, A., Jr., Schwasz, H.G., and Goldring, D.: J. Pediat. 66: 722, Levine, O.R., Jameson, A.G., Nellhaus, G., and Gold, A.P.: Pediatrics 30: 563, Montoya, G., Dohn, D.F., and Mercer, R.D.: Neurology 21: 1054, Fujishima, M.: Fukuoka Acta Med. 58: 194, Mori, H., Murakami, T., and Kawamata, K.: Jap. J. Clin. Exp. Med. 38: 570, Mori, H.: Jap. J. Clin. Exp. Med. 45: 371, Cabrera, E. and Monroy, J.R.: Am. Heart J. 43: 669, Atarashi, J., Yoshimura, M., Wada, Y., et al.: Clin. Neurol. 3: 252, Shenkin, H.A., Spitz, E.B., Grant, F.C., and Kety, S.S.: J. Neurosurg. 5: 165, Tonnis, W., Schiefer, W., and Walter, W.: J. Neurosurg. 15: 471, Wallace, J.M., Nashold, B.S., and Slewka, A.P.: Circulation. 31: 696, Lassen, N.A. and Munck, O.: Acta Psychiat. Neurol. Scand. 31: 71, Ray, B.S.: Surg. Gyne. Obst. 73: 615, Eichna, L.W.: Circulation. 22: 864, 1960.
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