This site uses cookies, tags, and tracking settings to store information that help give you the very best browsing experience. Dismiss this warning

Experimental investigation of encephalomyosynangiosis using gyrencephalic brain of the miniature pig: histopathological evaluation of dynamic reconstruction of vessels for functional anastomosis

Laboratory investigation

Mitsunobu Nakamura Departments of Neurosurgery and

Search for other papers by Mitsunobu Nakamura in
jns
Google Scholar
PubMed
Close
 M.D.
,
Hideaki Imai Departments of Neurosurgery and

Search for other papers by Hideaki Imai in
jns
Google Scholar
PubMed
Close
 M.D., Ph.D.
,
Kenjiro Konno Institute of Experimental Animal Research, Gunma University Graduate School of Medicine, Maebashi; and

Search for other papers by Kenjiro Konno in
jns
Google Scholar
PubMed
Close
 Ph.D.
,
Chisato Kubota Departments of Neurosurgery and

Search for other papers by Chisato Kubota in
jns
Google Scholar
PubMed
Close
 M.S.
,
Koji Seki Departments of Neurosurgery and

Search for other papers by Koji Seki in
jns
Google Scholar
PubMed
Close
 Ph.D.
,
Sandra Puentes Departments of Neurosurgery and

Search for other papers by Sandra Puentes in
jns
Google Scholar
PubMed
Close
 M.D.
,
Ahmad Faried Departments of Neurosurgery and

Search for other papers by Ahmad Faried in
jns
Google Scholar
PubMed
Close
 M.D., Ph.D.
,
Hideaki Yokoo Human Pathology, and

Search for other papers by Hideaki Yokoo in
jns
Google Scholar
PubMed
Close
 M.D., Ph.D.
,
Hidekazu Hata Institute of Experimental Animal Research, Gunma University Graduate School of Medicine, Maebashi; and

Search for other papers by Hidekazu Hata in
jns
Google Scholar
PubMed
Close
 Ph.D.
,
Yuhei Yoshimoto Departments of Neurosurgery and

Search for other papers by Yuhei Yoshimoto in
jns
Google Scholar
PubMed
Close
 M.D., Ph.D.
, and
Nobuhito Saito Department of Neurosurgery, Tokyo University Graduate School of Medicine, Tokyo, Japan

Search for other papers by Nobuhito Saito in
jns
Google Scholar
PubMed
Close
 M.D., Ph.D.
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $536.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $636.00
USD  $45.00
USD  $536.00
USD  $636.00
Print or Print + Online Sign in

Object

Encephalomyosynangiosis (EMS) is a surgical treatment for moyamoya disease that is widely used to provide increased intracranial blood flow via revascularization by arterial anastomosis from the external carotid artery. However, the angiogenic mechanism responsible for the revascularization induced by EMS has not been systematically evaluated. In this study the authors investigated the chronological angiogenic changes associated with EMS to clarify the favorable factors and identify revascularization mechanisms by using an experimental internal carotid artery occlusion (ICAO) model in the miniature pig.

Methods

Fourteen miniature pigs were used, 11 of which underwent ICAO before transcranial surgery for EMS was performed. Animals were allowed to recover for 1 week (4 pigs) or 4 weeks (7 pigs) after EMS. Control group animals were treated in the same way, but without occlusion (3 pigs). Magnetic resonance imaging, angiography, and histological investigation were performed.

Results

One week after EMS, on histological examination of both the ICAO and control groups it was found that the transplanted temporal muscle had adhered to the arachnoid via a granulation zone, which was enriched with immune cells such as macrophages associated with the angiogenic process. Four weeks after EMS, angiography and histological examination of the ICAO group showed patent anastomoses between the external carotid artery and the cortical arteries without any detectable boundary between the temporal muscle and the cerebral cortex. In contrast, histological examination of the control group found scar tissue between the cerebral cortex and temporal muscle.

Conclusions

The initial step for formation of anastomoses resembles the process of wound healing associated with repair processes such as active proliferation of macrophages and angiogenesis within the new connective tissue. Functional revascularization requires a suitable environment (such as tissue containing vascular beds) and stimulus (such as ischemia) to induce vascular expansion.

Abbreviations used in this paper:

CCA = common carotid artery; DW = diffusion weighted; ECA = external carotid artery; EMS = encephalomyosynangiosis; ICA = internal carotid artery; ICAO = ICA occlusion; MA = maxillary artery; MCA = middle cerebral artery; NEX = number of excitations; OA = occipital artery; PBS = phosphate-buffered saline; STA = superficial temporal artery.
  • Collapse
  • Expand
  • 1

    Buschmann I, & Schaper W: Arteriogenesis versus angiogenesis: two mechanisms of vessel growth. News Physiol Sci 14:121125, 1999

  • 2

    Cai WJ, , Koltai S, , Kocsis E, , Scholz D, , Kostin S, & Luo X, et al.: Remodeling of the adventitia during coronary arteriogenesis. Am J Physiol Heart Circ Physiol 284:H31H40, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Coussens LM, & Werb Z: Inflammation and cancer. Nature 420:860867, 2002

  • 4

    Gabbiani G: The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 200:500503, 2003

  • 5

    Goda M, , Isono M, , Ishii K, , Kamida T, , Abe T, & Kobayashi H, et al.: Long-term effects of indirect bypass surgery on collateral vessel formation in pediatric moyamoya disease. J Neurosurg 100:156162, 2004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Goldsmith HS, , Duckett S, & Chen WF: Prevention of cerebral infarction in the dog by intact omentum. Am J Surg 130:317320, 1975

  • 7

    Haaland K, , Orderud WJ, & Thoresen M: The piglet as a model for cerebral circulation: an angiographic study. Biol Neonate 68:7580, 1995

  • 8

    Heil M, , Eitenmuller I, , Schmitz-Rixen T, & Schaper W: Arteriogenesis versus angiogenesis: similarities and differences. J Cell Mol Med 10:4555, 2006

  • 9

    Houkin K, , Kamiyama H, , Takahashi A, , Kuroda S, & Abe H: Combined revascularization surgery for childhood moyamoya disease: STA-MCA and encephalo-duro-arterio-myosynangiosis. Childs Nerv Syst 13:2429, 1997

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Houkin K, , Kuroda S, , Ishikawa T, & Abe H: Neovascularization (angiogenesis) after revascularization in moyamoya disease. Which technique is most useful for moyamoya disease?. Acta Neurochir (Wien) 142:269276, 2000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Imai H, , Konno K, , Nakamura M, , Shimizu T, , Kubota C, & Seki K, et al.: A new model of focal cerebral ischemia in the miniature pig. J Neurosurg 104:2 Suppl 123132, 2006

  • 12

    Karasawa J, , Kikuchi H, , Furuse S, , Kawamura J, & Sakaki T: Treatment of moyamoya disease with STA-MCA anastomosis. J Neurosurg 49:679688, 1978

  • 13

    Karasawa J, , Kikuchi H, , Furuse S, , Sakaki T, & Yoshida Y: A surgical treatment of “moyamoya” disease “encephalo-myo synangiosis. Neurol Med Chir (Tokyo) 17:2937, 1977

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Kono S, , Oka K, , Sueishi K, & Sonobe M: Histopathological studies on spontaneous vault moyamoya and revascularized collaterals formed by encephalomyosynangiosis. Clin Neurol Neurosurg 99:Suppl 2 S209S212, 1997

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Kusaka N, , Sugiu K, , Tokunaga K, , Katsumata A, , Nishida A, & Namba K, et al.: Enhanced brain angiogenesis in chronic cerebral hypoperfusion after administration of plasmid human vascular endothelial growth factor in combination with indirect vasoreconstructive surgery. J Neurosurg 103:882890, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Masumori Y, , Nagashima C, & Nakamura H: Experimental omento-myelo-synangiosis. Surg Neurol 38:411417, 1992

  • 17

    Matsushima Y, , Takasato Y, , Fukumoto T, , Tsuruoka S, , Yamaguchi T, & Inaba Y: A case of internal carotid artery occlusion successfully treated by encephalo-duro-arterio-synangiosis. Childs Nerv Syst 1:363366, 1985

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Oberringer M, , Meins C, , Bubel M, & Pohlemann T: In vitro wounding: effects of hypoxia and transforming growth factor beta(1) on proliferation, migration and myofibroblastic differentiation in an endothelial cell-fibroblast co-culture model. J Mol Histol 39:3747, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Reinert M, , Brekenfeld C, , Taussky P, , Andres R, , Barth A, & Seiler RW, et al.: Cerebral revascularization model in a swine. Acta Neurochir Suppl 94:153157, 2005

  • 20

    Scholz D, , Ito W, , Fleming I, , Deindl E, , Sauer A, & Wiesnet M, et al.: Ultrastructure and molecular histology of rabbit hind-limb collateral artery growth (arteriogenesis). Virchows Arch 436:257270, 2000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Scott RM, , Smith JL, , Robertson RL, , Madsen JR, , Soriano SG, & Rockoff MA: Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg 100:2 Suppl Pediatrics 142149, 2004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Shimizu T, , Imai H, , Seki K, , Tomizawa S, , Nakamura M, & Honda F, et al.: Cyclophilin C-associated protein and cyclophilin C mRNA are upregulated in penumbral neurons and microglia after focal cerebral ischemia. J Cereb Blood Flow Metab 25:325337, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Sunderkotter C, , Steinbrink K, , Goebeler M, , Bhardwaj R, & Sorg C: Macrophages and angiogenesis. J Leukoc Biol 55:410422, 1994

  • 24

    Suzuki J, & Takaku A: Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288299, 1969

  • 25

    Tanaka Y, , Imai H, , Konno K, , Miyagishima T, , Kubota C, & Puentes S, et al.: Experimental model of lacunar infarction in the gyrencephalic brain of the miniature pig: neurological assessment and histological, immunohistochemical, and physiological evaluation of dynamic corticospinal tract deformation. Stroke 39:205212, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Touho H: A simple surgical technique of direct anastomosis for treatment of moyamoya disease: technical note. Surg Neurol 62:366368, 2004

  • 27

    Waltenberger J, , Kranz A, & Beyer M: Neovascularization in the human heart is associated with expression of VEGF-A and its receptors Flt-1 (VEGFR-1) and KDR (VEGFR-2). Results from cardiomyopexy in ischemic cardiomyopathy. Angiogenesis 3:345351, 1999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Warren GL, , Summan M, , Gao X, , Chapman R, , Hulderman T, & Simeonova PP, et al.: Mechanisms of skeletal muscle injury and repair revealed by gene expression studies in mouse models. J Physiol 582:825841, 2007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 1314 149 11
Full Text Views 268 27 3
PDF Downloads 198 24 1
EPUB Downloads 0 0 0