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01-06-2021 | Patent Ductus Arteriosus | Original Article

Cardiac manifestations in a western moyamoya disease population: a single-center descriptive study and review

Authors: Anthony S. Larson, Luis Savastano, James Klaas, Giuseppe Lanzino

Published in: Neurosurgical Review | Issue 3/2021

Abstract

An embryological association between moyamoya disease (MMD) and cardiac manifestations has been proposed. Data up to this point remains anecdotal, and the prevalence of cardiac manifestations in a western MMD population is uncertain. The objective of this study was to determine the prevalence of cardiac manifestations including coronary artery disease (CAD) and congenital cardiac defects in a mostly Caucasian population of MMD patients and review prior reports of such cases. Medical records of MMD patients who presented to our institution between 1990 and 2019 were retrospectively reviewed for the presence of various congenital cardiac malformations and concomitant CAD. The prevalence of congenital cardiac defects and CAD was determined. A literature search for prior cases of MMD with concomitant cardiac manifestations was performed. A total of 181 MMD patients were included in our analysis, 139 (76.8%) of whom were Caucasian. Ten patients had cardiac manifestations (5.5%). There were six total MMD patients with congenital cardiac defects (3.3%). All patients with congenital defects were diagnosed in childhood. The prevalence of congenital defects in MMD was slightly higher than the general population as reported previously (0.8–1.2%). Four MMD patients had CAD (2.2%). The mean age of patients with CAD was 41.0 years (SD = 12.3, range = 33–59) in our series and 33.1 years (SD = 15.0) in a review of prior reports. These mean ages of CAD are in contrast to the 7th and 8th decades of lifein the general population as indicated by prior studies. Our findings support an association between MMD and cardiac manifestations. Further investigation is warranted in order to further characterize this potential relationship and shed light on a possible cardio-cephalic neural crest syndrome.

Ahn YK, Jeong MH, Bom HS, Park JC, Kim JK, Chung DJ, Chung MY, Cho JG, Kang JC (1999) Myocardial infarction with moyamoya disease and pituitary gigantism in a young female patient. Jpn Circ J 63:644–648. https://doi.org/10.1253/jcj.63.644CrossRefPubMed

Akasaki T, Kagiyama S, Omae T, Ohya Y, Ibayashi S, Abe I, Fujishima M (1998) Asymptomatic moyamoya disease associated with coronary and renal artery stenoses--a case report. Jpn Circ J 62:136–138. https://doi.org/10.1253/jcj.62.136CrossRefPubMed

Arima Y, Miyagawa-Tomita S, Maeda K, Asai R, Seya D, Minoux M, Rijli FM, Nishiyama K, Kim KS, Uchijima Y, Ogawa H, Kurihara Y, Kurihara H (2012) Preotic neural crest cells contribute to coronary artery smooth muscle involving endothelin signalling. Nat Commun 3:1267. https://doi.org/10.1038/ncomms2258CrossRefPubMed

Babaoglu K, Demir T, Saltik L, Kutlug S, Islak C (2007) Moyamoya disease and aortic coarctation in a patient with common brachiocephalic trunk. Anadolu Kardiyol Derg 7:85–87PubMed

Baltaxe HA, Bloch S, Mooring PK (1982) Coarctation of the thoracic aorta associated with cerebral arterial occlusive disease. AJR Am J Roentgenol 139:1226–1229. https://doi.org/10.2214/ajr.139.6.1226CrossRefPubMed

Benjamin EJ, Blaha MJ, Chiuve SE, Cushman M, Das SR, Deo R, de Ferranti SD, Floyd J, Fornage M, Gillespie C, Isasi CR, Jimenez MC, Jordan LC, Judd SE, Lackland D, Lichtman JH, Lisabeth L, Liu S, Longenecker CT, Mackey RH, Matsushita K, Mozaffarian D, Mussolino ME, Nasir K, Neumar RW, Palaniappan L, Pandey DK, Thiagarajan RR, Reeves MJ, Ritchey M, Rodriguez CJ, Roth GA, Rosamond WD, Sasson C, Towfighi A, Tsao CW, Turner MB, Virani SS, Voeks JH, Willey JZ, Wilkins JT, Wu JH, Alger HM, Wong SS, Muntner P, American Heart Association Statistics C, Stroke Statistics S (2017) Heart disease and stroke statistics-2017 update: a report from the American Heart Association. Circulation 135:e146–e603. https://doi.org/10.1161/CIR.0000000000000485CrossRefPubMedPubMedCentral

Chang SA, Song JS, Park TK, Yang JH, Kwon WC, Kim SR, Kim SM, Cha J, Jang SY, Cho YS, Kim TJ, Bang OY, Song JY, Ki CS, Kim DK (2018) Nonsyndromic peripheral pulmonary artery stenosis is associated with homozygosity of RNF213 p.Arg4810Lys regardless of co-occurrence of moyamoya disease. Chest 153:404–413. https://doi.org/10.1016/j.chest.2017.09.023CrossRefPubMed

Choi W, Kim YN, Kim KH (2015) Variant angina in moyamoya disease--a correlative etiology and different presentation: a case report. J Med Case Rep 9:86. https://doi.org/10.1186/s13256-015-0537-4CrossRefPubMedPubMedCentral

Coskun E, Altinay L, Tutun U, Tekin A (2018) Off-pump coronary artery bypass grafting in moyamoya disease: a case report. Braz J Cardiovasc Surg 33:309–311. https://doi.org/10.21470/1678-9741-2017-0219CrossRefPubMedPubMedCentral

10.

Etchevers HC, Vincent C, Le Douarin NM, Couly GF (2001) The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development 128:1059–1068CrossRef

11.

Furuta K, Homma T, Yoshioka J, Tamura Y, Hirabayashi H, Sasaki Y, Kawa S, Monno S, Hara T, Furuta S (1985) A case of moyamoya disease associated with stenosis of the right coronary artery, sick sinus syndrome and hypertrophic cardiomyopathy. Kokyu To Junkan 33:1401–1406PubMed

12.

Ganesan V, Kirkham FJ (1997) Noonan syndrome and moyamoya. Pediatr Neurol 16:256–258. https://doi.org/10.1016/s0887-8994(97)89980-8CrossRefPubMed

13.

Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Magid D, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Nichol G, Paynter NP, Schreiner PJ, Sorlie PD, Stein J, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics C, Stroke Statistics S (2013) Heart disease and stroke statistics--2013 update: a report from the American Heart Association. Circulation 127:e6–e245. https://doi.org/10.1161/CIR.0b013e31828124adCrossRefPubMed

14.

Grangeon L, Guey S, Schwitalla JC, Bergametti F, Arnould M, Corpechot M, Hadjadj J, Riant F, Aloui C, Drunat S, Vidaud D, Tournier-Lasserve E, Kraemer M (2019) Clinical and molecular features of 5 European multigenerational families with moyamoya angiopathy. Stroke 50:789–796. https://doi.org/10.1161/STROKEAHA.118.023972CrossRefPubMed

15.

Herve D, Touraine P, Verloes A, Miskinyte S, Krivosic V, Logeart D, Alili N, Laredo JD, Gaudric A, Houdart E, Metzger JP, Tournier-Lasserve E, Woimant F (2010) A hereditary moyamoya syndrome with multisystemic manifestations. Neurology 75:259–264. https://doi.org/10.1212/WNL.0b013e3181e8ee3fCrossRefPubMed

16.

Hoshimaru M, Takahashi JA, Kikuchi H, Nagata I, Hatanaka M (1991) Possible roles of basic fibroblast growth factor in the pathogenesis of moyamoya disease: an immunohistochemical study. J Neurosurg 75:267–270. https://doi.org/10.3171/jns.1991.75.2.0267CrossRefPubMed

17.

Ikeda U, Fujikawa H, Shimada K (1998) Variant angina pectoris associated with moyamoya disease. Lancet 351:183–184. https://doi.org/10.1016/S0140-6736(98)24003-7CrossRefPubMed

18.

Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A, Kanno J, Niihori T, Ono M, Ishii N, Owada Y, Fujimura M, Mashimo Y, Suzuki Y, Hata A, Tsuchiya S, Tominaga T, Matsubara Y, Kure S (2011) A genome-wide association study identifies RNF213 as the first moyamoya disease gene. J Hum Genet 56:34–40. https://doi.org/10.1038/jhg.2010.132CrossRefPubMed

19.

Kim DK, Yoo KJ (2007) Off-pump coronary artery bypass grafting in moyamoya disease. Yonsei Med J 48:876–878. https://doi.org/10.3349/ymj.2007.48.5.876CrossRefPubMedPubMedCentral

20.

Kim EH, Yum MS, Ra YS, Park JB, Ahn JS, Kim GH, Goo HW, Ko TS, Yoo HW (2016) Importance of RNF213 polymorphism on clinical features and long-term outcome in moyamoya disease. J Neurosurg 124:1221–1227. https://doi.org/10.3171/2015.4.JNS142900CrossRefPubMed

21.

Kim S, Park C, Han S, Park S, Kim J, Park S, Choi J, Choi C, Ahn J, Seo H, Oh D (2002) A case of moyamoya disease with total occlusion of left main coronary artery. Korean Circ J 32:275–279CrossRef

22.

Kobayashi H, Brozman M, Kyselova K, Viszlayova D, Morimoto T, Roubec M, Skoloudik D, Petrovicova A, Juskanic D, Strauss J, Halaj M, Kurray P, Hranai M, Harada KH, Inoue S, Yoshida Y, Habu T, Herzig R, Youssefian S, Koizumi A (2016) RNF213 rare variants in Slovakian and Czech moyamoya disease patients. PLoS One 11:e0164759. https://doi.org/10.1371/journal.pone.0164759CrossRefPubMedPubMedCentral

23.

Komiyama M (2017) Cardio-cephalic neural crest syndrome: a novel hypothesis of vascular neurocristopathy. Interv Neuroradiol 23:572–576. https://doi.org/10.1177/1591019917726093CrossRefPubMedPubMedCentral

24.

Komiyama M (2017) Moyamoya disease is a vascular form of neurocristopathy: disease of the embryologic cephalic neural crest. Childs Nerv Syst 33:567–568. https://doi.org/10.1007/s00381-017-3369-2CrossRefPubMed

25.

Komiyama M, Ishikawa T, Takanashi S, Shimizu Y (2003) Minimal invasive direct coronary artery bypass in moyamoya disease. Interact Cardiovasc Thorac Surg 2:65–67. https://doi.org/10.1016/S1569-9293(02)00100-7CrossRefPubMed

26.

Komiyama M, Nishikawa M, Yasui T, Otsuka M, Haze K (2001) Moyamoya disease and coronary artery disease--case report. Neurol Med Chir (Tokyo) 41:37–41. https://doi.org/10.2176/nmc.41.37CrossRef

27.

Korematsu K, Yoshioka S, Maruyama T, Nagai Y, Inoue K, Yukaya N, Baba H, Kuratsu J (2007) Moyamoya disease associated with midaortic syndrome. Pediatr Neurosurg 43:54–59. https://doi.org/10.1159/000097528CrossRefPubMed

28.

Kraemer M, Schwitalla JC, Diesner F, Aktas O, Hartung HP, Berlit P (2019) Clinical presentation of moyamoya angiopathy in Europeans: experiences from Germany with 200 patients. J Neurol 266:1421–1428. https://doi.org/10.1007/s00415-019-09277-1CrossRefPubMed

29.

Larson A, Rinaldo L, Brinjikji W, Klaas J, Lanzino G (2020) Intracranial vessel stenosis in a young patient with an MYH11 mutation: a case report and review of 2 prior cases. World Neurosurg 137:243–246. https://doi.org/10.1016/j.wneu.2020.02.054CrossRefPubMed

30.

Le Douarin NM, Kalcheim C (1999) The neural crest. Developmental and cell biology, 2nd edn. Cambridge University Press, CambridgeCrossRef

31.

Lee JH, Youn TJ, Yoon YE, Park JJ, Hong SJ, Chun EJ, Choi SI, Cho YS, Cho GY, Chae IH, Choi DJ (2013) Coronary artery stenosis in moyamoya disease: tissue characterization by 256-slice multi-detector CT and virtual histology. Circulation 127:2063–2065. https://doi.org/10.1161/CIRCULATIONAHA.112.136473CrossRefPubMed

32.

Liu W, Morito D, Takashima S, Mineharu Y, Kobayashi H, Hitomi T, Hashikata H, Matsuura N, Yamazaki S, Toyoda A, Kikuta K, Takagi Y, Harada KH, Fujiyama A, Herzig R, Krischek B, Zou L, Kim JE, Kitakaze M, Miyamoto S, Nagata K, Hashimoto N, Koizumi A (2011) Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PLoS One 6:e22542. https://doi.org/10.1371/journal.pone.0022542CrossRefPubMedPubMedCentral

33.

Lutterman J, Scott M, Nass R, Geva T (1998) Moyamoya syndrome associated with congenital heart disease. Pediatrics 101:57–60. https://doi.org/10.1542/peds.101.1.57CrossRefPubMed

34.

Marelli AJ, Mackie AS, Ionescu-Ittu R, Rahme E, Pilote L (2007) Congenital heart disease in the general population: changing prevalence and age distribution. Circulation 115:163–172. https://doi.org/10.1161/CIRCULATIONAHA.106.627224CrossRefPubMed

35.

Marino B, Vairo U, Corno A, Nava S, Guccione P, Calabro R, Marcelletti C (1990) Atrioventricular canal in Down syndrome. Prevalence of associated cardiac malformations compared with patients without Down syndrome. Am J Dis Child 144:1120–1122. https://doi.org/10.1001/archpedi.1990.02150340066025CrossRefPubMed

36.

Mitchell SC, Korones SB, Berendes HW (1971) Congenital heart disease in 56,109 births. Incidence and natural history. Circulation 43:323–332. https://doi.org/10.1161/01.cir.43.3.323CrossRefPubMed

37.

Miyatake S, Miyake N, Touho H, Nishimura-Tadaki A, Kondo Y, Okada I, Tsurusaki Y, Doi H, Sakai H, Saitsu H, Shimojima K, Yamamoto T, Higurashi M, Kawahara N, Kawauchi H, Nagasaka K, Okamoto N, Mori T, Koyano S, Kuroiwa Y, Taguri M, Morita S, Matsubara Y, Kure S, Matsumoto N (2012) Homozygous c.14576G>A variant of RNF213 predicts early-onset and severe form of moyamoya disease. Neurology 78:803–810. https://doi.org/10.1212/WNL.0b013e318249f71fCrossRefPubMed

38.

Morimoto T, Mineharu Y, Ono K, Nakatochi M, Ichihara S, Kabata R, Takagi Y, Cao Y, Zhao L, Kobayashi H, Harada KH, Takenaka K, Funaki T, Yokota M, Matsubara T, Yamamoto K, Izawa H, Kimura T, Miyamoto S, Koizumi A (2017) Significant association of RNF213 p.R4810K, a moyamoya susceptibility variant, with coronary artery disease. PLoS One 12:e0175649. https://doi.org/10.1371/journal.pone.0175649CrossRefPubMedPubMedCentral

39.

Munot P, Saunders DE, Rittey C, Philip S, Jacques TS, Agrawal S, Ganesan V (2011) Multisystem smooth muscle dysfunction due to novel mutations in ACTA2: a phenotype presenting to neurologists with distinct cerebrovascular features. Dev Med Child Neurol 1:56–57. https://doi.org/10.1111/j.1469-8749.2010.03866.xCrossRef

40.

Murakami T, Ueno M, Takeda A, Yakuwa S, Kuroda S (2009) Image in cardiovascular medicine. Multiple coronary stenosis in infantile moyamoya disease. Circulation 119:1689. https://doi.org/10.1161/CIRCULATIONAHA.108.827782CrossRefPubMed

41.

Nam TM, Jo KI, Yeon JY, Hong SC, Kim JS (2015) Coronary heart disease in moyamoya disease: are they concomitant or coincidence? J Korean Med Sci 30:470–474. https://doi.org/10.3346/jkms.2015.30.4.470CrossRefPubMedPubMedCentral

42.

Natori Y, Ikezaki K, Matsushima T, Fukui M (1997) ‘Angiographic moyamoya’ its definition, classification, and therapy. Clin Neurol Neurosurg 99(Suppl 2):S168–S172. https://doi.org/10.1016/s0303-8467(97)00052-8CrossRefPubMed

43.

Okamoto Y, Minakata K, Katsu M (2010) Off-pump coronary artery bypass grafting supported by intra-aortic balloon pumping in a patient with moyamoya disease. Kyobu Geka 63:1057–1060PubMed

44.

Research Committee on the P, Treatment of Spontaneous Occlusion of the Circle of W, Health Labour Sciences Research Grant for Research on Measures for Infractable D (2012) Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245–266. https://doi.org/10.2176/nmc.52.245CrossRef

45.

Roberts AE, Allanson JE, Tartaglia M, Gelb BD (2013) Noonan syndrome. Lancet 381:333–342. https://doi.org/10.1016/S0140-6736(12)61023-XCrossRefPubMedPubMedCentral

46.

Saito K, Hirano H, Katsumata U, Sato K, Matsumoto N, Onodera Y, Miura T, Iwabuchi T, Taakasugi R (1987) A case presenting an intracranial hemorrhage due to moyamoya disease in association with stenosis of the anterior descending branch of the left coronary artery. Jpn Circ J 51:24

47.

Sakamoto K, Matsumoto M, Miyamoto N, Kounaka S, Okimoto T, Dohi Y (1987) A case of angina pectoris with moyamoya-like cerebro-vascular lesions. Jpn Circ J 51:239

48.

Sanchis-Gomar F, Perez-Quilis C, Leischik R, Lucia A (2016) Epidemiology of coronary heart disease and acute coronary syndrome. Ann Transl Med 4:256. https://doi.org/10.21037/atm.2016.06.33CrossRefPubMedPubMedCentral

49.

Schuster JM, Roberts TS (1999) Symptomatic moyamoya disease and aortic coarctation in a patient with Noonan’s syndrome: strategies for management. Pediatr Neurosurg 30:206–210. https://doi.org/10.1159/000028797CrossRefPubMed

50.

Scott RM, Smith ER (2009) Moyamoya disease and moyamoya syndrome. N Engl J Med 360:1226–1237. https://doi.org/10.1056/NEJMra0804622CrossRefPubMed

51.

Shiratori K, Akasaka T, Asaka T, Shibuya Y, Suzuki K, Yoshida K, Koizumi K, Okumachi F, Yanagihara K, Kato H, Yoshikawa J (1985) A case of a young woman with occlusion of the circle of Willis (moyamoya disease) presenting with angina pectoris. Jpn Circ J 49:112

52.

St Goar FG, Gominak SC, Potkin BN (1999) Bilateral aortoostial coronary artery disease: moyamoya of the heart? Am J Cardiol 83(1296–1299):A1210–A1299. https://doi.org/10.1016/s0002-9149(99)00081-8CrossRef

53.

Suzuki K, Kawarada U, Takeuchi N, Mine T, Ooneda G, Takatama M (1989) An autopsy case of moyamoya disease died of acute heart failure. Gunma Igaku 50:211–214

54.

Tateno M, Oono T, Ooshima N, Kato N, Tsukada H, Iwasaki T, Sakurai F, Sasaki T, Kanazawa N, Takeuchi H (1988) A case of a young woman with moyamoya disease presenting angina pectoris. Nippon Naika Gakkai Zasshi 77:100

55.

Togao O, Mihara F, Yoshiura T, Tanaka A, Kuwabara Y, Morioka T, Matsushima T, Sasaki T, Honda H (2004) Prevalence of stenoocclusive lesions in the renal and abdominal arteries in moyamoya disease. AJR Am J Roentgenol 183:119–122. https://doi.org/10.2214/ajr.183.1.1830119CrossRefPubMed

56.

Tokunaga Y, Toyoda K, Ago T, Ibayashi S, Usui M, Fujishima M (1996) Systemic vascular change associated with moyamoya-like cerebrovascular disease and microvascular coronary artery disease. Rinsho Shinkeigaku 36:318–322PubMed

57.

von Bary C, Liebig T, Gaa J, von Beckerath N (2008) Ischaemic stroke and myocardial infarction in a Caucasian patient with moya-moya disease. Eur Heart J 29:842. https://doi.org/10.1093/eurheartj/ehm513CrossRef

58.

Wang Y, Zhang Z, Wei L, Zhang Q, Zou Z, Yang L, Li D, Shang M, Han C, Mambiya M, Bao X, Li Q, Hao F, Zhang K, Wang H, Liu S, Liu M, Zeng F, Nie F, Wang K, Liu W, Duan L (2020) Predictive role of heterozygous p.R4810K of RNF213 in the phenotype of Chinese moyamoya disease. Neurology 94:e678–e686. https://doi.org/10.1212/WNL.0000000000008901CrossRefPubMedPubMedCentral

59.

Yamashita M, Oka K, Tanaka K (1983) Histopathology of the brain vascular network in moyamoya disease. Stroke 14:50–58. https://doi.org/10.1161/01.str.14.1.50CrossRefPubMed

60.

Yamashita M, Tanaka K, Kishikawa T, Yokota K (1984) Moyamoya disease associated with renovascular hypertension. Hum Pathol 15:191–193. https://doi.org/10.1016/s0046-8177(84)80060-xCrossRefPubMed

61.

Zheng YM, Xie CH, Gong FQ (2014) Moyamoya disease associated with aortic coarctation. World J Pediatr 10:374. https://doi.org/10.1007/s12519-014-0516-7CrossRefPubMed

Title: Cardiac manifestations in a western moyamoya disease population: a single-center descriptive study and review
Authors: Anthony S. Larson
Luis Savastano
James Klaas
Giuseppe Lanzino
Publication date: 01-06-2021
Publisher: Springer Berlin Heidelberg
Keywords: Patent Ductus Arteriosus
Patent Ductus Arteriosus
Patent Ductus Arteriosus
Patent Ductus Arteriosus
Arterial Diseases
Published in: Neurosurgical Review / Issue 3/2021
Print ISSN: 0344-5607
Electronic ISSN: 1437-2320
DOI: https://doi.org/10.1007/s10143-020-01327-x

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Cardiac manifestations in a western moyamoya disease population: a single-center descriptive study and review

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