Anomaly in aortic arch alters pathological outcome of transient global ischemia in Rhesus macaques

Koichi Hara, Takao Yasuhara, Mina Maki, Noriyuki Matsukawa, Guolong Yu, Lin Xu, Laura Tambrallo, Nancy A. Rodriguez, David Stern, Tetsumori Yamashima, Jerry J. Buccafusco, Takeshi Kawase, David C. Hess, Cesario V. Borlongan

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

We investigated a non-human primate (NHP) transient global ischemia (TGI) model which was induced by clipping the arteries originating from the aortic arch. Previously we demonstrated that our TGI model in adult Rhesus macaques (Macaca mulatta) results in marked neuronal cell loss in the hippocampal region, specifically the cornu Ammonis (CA1) region. However, we observed varying degrees of hippocampal cell loss among animals. Here, we report for the first time an anomaly of the aortic arch in some Rhesus macaques that appears as a key surgical factor in ensuring the success of the TGI model in this particular NHP. Eleven adult Rhesus macaques underwent the TGI surgery, which involved 10-15-minute clipping of both innominate and subclavian arteries. Animals were allowed to survive between 1 day and 28 days after TGI. Because of our experience and knowledge that Japanese macaques exhibited only innominate and subclavian arteries arising from the aortic arch, macroscopic visualization of these two arteries alone in the Rhesus macaques initially assured us that clipping both arteries was sufficient to produce TGI. During the course of one TGI operation, however, we detected 3 arterial branches arising from the aortic arch, which prompted us to subsequently search for 3 branches in succeeding TGI surgeries. In addition, we performed post-mortem examination of the heart to confirm the number of arterial branches in the aortic arch. Finally, in order to reveal the pathological effect of the aortic arch anomaly, we compared the hippocampal cell loss between animals found to have 3 arterial branches but had all or only two branches clipped during TGI operation. Post-mortem examination revealed that eight NHPs had the typical two arterial aortic branches, but three NHPs displayed an extra arterial aortic branch, indicating that about 30% of Rhesus macaques had 3 arterial branches arising from the aorta. Histological analyses using Nissl staining showed that in NHPs with the aortic arch anomaly clipping only two of three arterial branches led to a partial cell loss and minimal alteration in number of cell layers in the hippocampal region when compared with clipping all three branches, with the hippocampal cell death in the latter resembling the pathological outcome achieved by clipping the two arterial branches in NHPs displaying the typical two-artery aortic arch. The finding that 3 of 11 NHPs exhibited an extra arterial aortic branch recognizes this aortic arch anomaly in Rhesus macaques that warrants a critical surgical maneuver in order to successfully produce consistent TGI-induced hippocampal cell loss.

Original languageEnglish (US)
Pages (from-to)185-191
Number of pages7
JournalBrain Research
Volume1286
DOIs
StatePublished - Aug 25 2009
Externally publishedYes

Fingerprint

Macaca mulatta
Thoracic Aorta
Ischemia
Arteries
Brachiocephalic Trunk
Subclavian Artery
Primates
Autopsy
Macaca
Aorta
Hippocampus
Cell Death
Cell Count
Staining and Labeling

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Molecular Biology
  • Developmental Biology
  • Clinical Neurology

Cite this

Hara, K., Yasuhara, T., Maki, M., Matsukawa, N., Yu, G., Xu, L., ... Borlongan, C. V. (2009). Anomaly in aortic arch alters pathological outcome of transient global ischemia in Rhesus macaques. Brain Research, 1286, 185-191. https://doi.org/10.1016/j.brainres.2009.06.015

Anomaly in aortic arch alters pathological outcome of transient global ischemia in Rhesus macaques. / Hara, Koichi; Yasuhara, Takao; Maki, Mina; Matsukawa, Noriyuki; Yu, Guolong; Xu, Lin; Tambrallo, Laura; Rodriguez, Nancy A.; Stern, David; Yamashima, Tetsumori; Buccafusco, Jerry J.; Kawase, Takeshi; Hess, David C.; Borlongan, Cesario V.

In: Brain Research, Vol. 1286, 25.08.2009, p. 185-191.

Research output: Contribution to journalArticle

Hara, K, Yasuhara, T, Maki, M, Matsukawa, N, Yu, G, Xu, L, Tambrallo, L, Rodriguez, NA, Stern, D, Yamashima, T, Buccafusco, JJ, Kawase, T, Hess, DC & Borlongan, CV 2009, 'Anomaly in aortic arch alters pathological outcome of transient global ischemia in Rhesus macaques', Brain Research, vol. 1286, pp. 185-191. https://doi.org/10.1016/j.brainres.2009.06.015
Hara, Koichi ; Yasuhara, Takao ; Maki, Mina ; Matsukawa, Noriyuki ; Yu, Guolong ; Xu, Lin ; Tambrallo, Laura ; Rodriguez, Nancy A. ; Stern, David ; Yamashima, Tetsumori ; Buccafusco, Jerry J. ; Kawase, Takeshi ; Hess, David C. ; Borlongan, Cesario V. / Anomaly in aortic arch alters pathological outcome of transient global ischemia in Rhesus macaques. In: Brain Research. 2009 ; Vol. 1286. pp. 185-191.
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AU - Yu, Guolong

AU - Xu, Lin

AU - Tambrallo, Laura

AU - Rodriguez, Nancy A.

AU - Stern, David

AU - Yamashima, Tetsumori

AU - Buccafusco, Jerry J.

AU - Kawase, Takeshi

AU - Hess, David C.

AU - Borlongan, Cesario V.

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N2 - We investigated a non-human primate (NHP) transient global ischemia (TGI) model which was induced by clipping the arteries originating from the aortic arch. Previously we demonstrated that our TGI model in adult Rhesus macaques (Macaca mulatta) results in marked neuronal cell loss in the hippocampal region, specifically the cornu Ammonis (CA1) region. However, we observed varying degrees of hippocampal cell loss among animals. Here, we report for the first time an anomaly of the aortic arch in some Rhesus macaques that appears as a key surgical factor in ensuring the success of the TGI model in this particular NHP. Eleven adult Rhesus macaques underwent the TGI surgery, which involved 10-15-minute clipping of both innominate and subclavian arteries. Animals were allowed to survive between 1 day and 28 days after TGI. Because of our experience and knowledge that Japanese macaques exhibited only innominate and subclavian arteries arising from the aortic arch, macroscopic visualization of these two arteries alone in the Rhesus macaques initially assured us that clipping both arteries was sufficient to produce TGI. During the course of one TGI operation, however, we detected 3 arterial branches arising from the aortic arch, which prompted us to subsequently search for 3 branches in succeeding TGI surgeries. In addition, we performed post-mortem examination of the heart to confirm the number of arterial branches in the aortic arch. Finally, in order to reveal the pathological effect of the aortic arch anomaly, we compared the hippocampal cell loss between animals found to have 3 arterial branches but had all or only two branches clipped during TGI operation. Post-mortem examination revealed that eight NHPs had the typical two arterial aortic branches, but three NHPs displayed an extra arterial aortic branch, indicating that about 30% of Rhesus macaques had 3 arterial branches arising from the aorta. Histological analyses using Nissl staining showed that in NHPs with the aortic arch anomaly clipping only two of three arterial branches led to a partial cell loss and minimal alteration in number of cell layers in the hippocampal region when compared with clipping all three branches, with the hippocampal cell death in the latter resembling the pathological outcome achieved by clipping the two arterial branches in NHPs displaying the typical two-artery aortic arch. The finding that 3 of 11 NHPs exhibited an extra arterial aortic branch recognizes this aortic arch anomaly in Rhesus macaques that warrants a critical surgical maneuver in order to successfully produce consistent TGI-induced hippocampal cell loss.

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