Decreased 13N‑labeled ammonia uptake in the ipsilateral and contralateral hemispheres following carotid endarterectomy

Wang,Tao; Wang,Xuemei; He,Yulin; Zhang,Tao; Song,Jianqiang; Bai,Xia; Han,Chunlei

doi:10.3892/mmr.2015.4303

Decreased 13N‑labeled ammonia uptake in the ipsilateral and contralateral hemispheres following carotid endarterectomy

Authors:
- Tao Wang
- Xuemei Wang
- Yulin He
- Tao Zhang
- Jianqiang Song
- Xia Bai
- Chunlei Han
View Affiliations

Affiliations: Department of Neurosurgery, The Affiliated Hospital of Inner Mongolia Medical University, Hohhot, Inner Mongolia 010050, P.R. China, Department of Nuclear Medicine, The Affiliated Hospital of Inner Mongolia Medical University, Hohhot, Inner Mongolia 010050, P.R. China, Turku PET Center, Turku University Hospital, Turku 20520, Finland
Published online on: September 9, 2015 https://doi.org/10.3892/mmr.2015.4303
Pages: 6598-6604
Copyright: © Wang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Carotid artery plaques are a leading cause of ischemic stroke, and carotid endarterectomy (CEA) is one of the major treatment approaches for this disease. Changes in cerebral metabolism following CEA remain unclear. The present study aimed to evaluate the effect of cerebral ammonia metabolism following CEA using 13N‑labeled ammonia positron emission tomography (PET) in humans. A total of 20 patients were enrolled in the present study, with a mean age of 59.5 years, comprising 16 males and four females. Of these patients, eight underwent right CEA and 12 underwent left CEA. The rate of carotid artery stenosis was between 50‑69% in six of the patients, between 70‑99% in 11 of the patients and was at 100% (thrombosis) in three of the patients, measured by computerised tomography digital subtraction angiography prior to CEA. 13N‑labeled ammonia (137 MBq) PET scanning was performed prior and subsequent to CEA surgery for each patient. The first ammonia PET scan was performed 1 day prior to CEA, while the second PET scan was performed 1‑4 weeks following CEA. Following injection of 13N‑labeled ammonia, static PET was acquired for 10 min. The region of interest (ROI), covering the major cerebral hemisphere, was selected and ammonia uptake in the ROI was determined in the ipsilateral and contralateral hemispheres. No hyperperfusion syndrome was observed in the patients subsequent to CEA. No significant change in cerebral hemisphere ammonia uptake was observed between the ipsilateral and contralateral hemispheres prior to (ratio =0.98; P>0.01) or following (ratio =1.09; P>0.01) CEA. Ammonia uptake in the ipsilateral and contralateral hemispheres was significantly reduced to 23.2 and 23.5%, respectively, following CEA. Using 13N‑labeled ammonia PET to evaluate cerebral ammonia metabolism following CEA in patients with severe carotid artery stenosis, the present study demonstrated that uptake of ammonia in the ipsilateral and contralateral hemispheres was significantly reduced.

View Figures

View References

1	Silver FL, Mackey A, Clark WM, Brooks W, Timaran CH, Chiu D, Goldstein LB, Meschia JF, Ferguson RD, Moore WS, et al CREST Investigators: Safety of stenting and endarterectomy by symptomatic status in the carotid revascularization endarterectomy versus stenting trial (CREST). Stroke. 42:675–680. 2011. View Article : Google Scholar : PubMed/NCBI
2	Pennekamp CW, Immink RV, den Ruijter HM, Kappelle LJ, Ferrier CM, Bots ML, Buhre WF, Moll FL and de Borst GJ: Near-infrared spectroscopy can predict the onset of cerebral hyperperfusion syndrome after carotid endarterectomy. Cerebrovasc Dis. 34:314–321. 2012. View Article : Google Scholar : PubMed/NCBI
3	Russjan A, Goebell E, Havemeister S, Thomalla G, Cheng B, Beck C, Krützelmann A, Fiehler J, Gerloff C and Rosenkranz M: Predictors of periprocedural brain lesions associated with carotid stenting. Cerebrovasc Dis. 33:30–36. 2012. View Article : Google Scholar
4	Buczek J, Karliński M, Kobayashi A, Białek P and Członkowska: Hyperperfusion syndrome after carotid endarterectomy and carotid stenting. Cerebrovasc Dis. 35:531–537. 2013. View Article : Google Scholar : PubMed/NCBI
5	Mantese VA, Timaran CH, Chiu D, Begg RJ and Brott TG; CREST investigators: The Carotid Revascularization Endarterectomy versus Stenting Trial (CREST): Stenting versus carotid endarterectomy for carotid disease. Stroke. 41(Suppl): S31–S34. 2010. View Article : Google Scholar : PubMed/NCBI
6	Bond R, Rerkasem K, Cuffe R and Rothwell PM: A systematic review of the associations between age and sex and the operative risks of carotid endarterectomy. Cerebrovasc Dis. 20:69–77. 2005. View Article : Google Scholar : PubMed/NCBI
7	Saito H, Kuroda S, Hirata K, Magota K, Shiga T, Tamaki N, Yoshida D, Terae S, Nakayama N and Houkin K: Validity of dual MRI and F-FDG PET imaging in predicting vulnerable and inflamed carotid plaque. Cerebrovasc Dis. 35:370–377. 2013. View Article : Google Scholar : PubMed/NCBI
8	Nanba T, Ogasawara K, Nishimoto H, Fujiwara S, Kuroda H, Sasaki M, Kudo K, Suzuki T, Kobayashi M, Yoshida K and Ogawa A: Postoperative cerebral white matter damage associated with cerebral hyperperfusion and cognitive impairment after carotid endarterectomy: A diffusion tensor magnetic resonance imaging study. Cerebrovasc Dis. 34:358–367. 2012. View Article : Google Scholar : PubMed/NCBI
9	Vanninen E, Kuikka JT, Aikiä M, Könönen M and Vanninen R: Heterogeneity of cerebral blood flow in symptomatic patients undergoing carotid endarterectomy. Nucl Med Commun. 24:893–900. 2003. View Article : Google Scholar : PubMed/NCBI
10	Yang B, Chen W, Yang Y, Lin Y, Duan Y, Li J, Wang H, Fu F, Zhuge Q and Chen X: Short- and long-term hemodynamic and clinical effects of carotid artery stenting. AJNR Am J Neuroradiol. 33:1170–1176. 2012. View Article : Google Scholar : PubMed/NCBI
11	Trojanowska A, Drop A, Jargiello T, Wojczal J and Szczerbo-Trojanowska M: Changes in cerebral hemodynamics after carotid stenting: Evaluation with CT perfusion studies. J Neuroradiol. 33:169–174. 2006. View Article : Google Scholar : PubMed/NCBI
12	Rijbroek A, Boellaard R, Vermeulen EG, Lammertsma AA and Rauwerda JA: Hemodynamic changes in ipsi- and contralateral cerebral arterial territories after carotid endarterectomy using positron emission tomography. Surg Neurol. 71:668–676. 2009. View Article : Google Scholar
13	Gaudet JG, Meyers PM, McKinsey JF, Lavine SD, Gray W, Mitchell E, Connolly ES Jr and Heyer EJ: Incidence of moderate to severe cognitive dysfunction in patients treated with carotid artery stenting. Neurosurgery. 65:325–329. 2009. View Article : Google Scholar : PubMed/NCBI
14	Rothman DL, De Feyter HM, Maciejewski PK and Behar KL: Is there in vivo evidence for amino acid shuttles carrying ammonia from neurons to astrocytes? Neurochem Res. 37:2597–2612. 2012. View Article : Google Scholar : PubMed/NCBI
15	Adeva MM, Souto G, Blanco N and Donapetry C: Ammonium metabolism in humans. Metabolism. 61:1459–1511. 2012. View Article : Google Scholar
16	Cooper AJ: 13N as a tracer for studying glutamate metabolism. Neurochem Int. 59:456–464. 2011. View Article : Google Scholar :
17	Maes F, Collignon A, Vandermeulen D, Marchal G and Suetens P: Multimodality image registration by maximization of mutual information. IEEE Trans Med Imaging. 16:187–198. 1997. View Article : Google Scholar : PubMed/NCBI
18	Gröschel K, Schnaudigel S, Pilgram SM, Wasser K and Kastrup A: A systematic review on outcome after stenting for intracranial atherosclerosis. Stroke. 40:e340–e347. 2009. View Article : Google Scholar : PubMed/NCBI
19	Gahremanpour A, Perin EC and Silva G: Carotid artery stenting versus endarterectomy: A systematic review. Tex Heart Inst J. 39:474–487. 2012.PubMed/NCBI
20	Timaran CH, Mantese VA, Malas M, Brown OW, Lal BK, Moore WS, Voeks JH and Brott TG; CREST Investigators: Differential outcomes of carotid stenting and endarterectomy performed exclusively by vascular surgeons in the Carotid Revascularization Endarterectomy versus Stenting Trial (CREST). J Vasc Surg. 57:303–308. 2013. View Article : Google Scholar :
21	Araki CT, Babikian VL, Cantelmo NL and Johnson WC: Cerebrovascular hemodynamic changes associated with carotid endarterectomy. J Vasc Surg. 13:854–859. 1991. View Article : Google Scholar : PubMed/NCBI
22	Lin MS, Chiu MJ, Wu YW, Huang CC, Chao CC, Chen YH, Lin HJ, Li HY, Chen YF, Lin LC, et al: Neurocognitive improvement after carotid artery stenting in patients with chronic internal carotid artery occlusion and cerebral ischemia. Stroke. 42:2850–2854. 2011. View Article : Google Scholar : PubMed/NCBI
23	Mendiz OA, Sposato LA, Fabbro N, Lev GA, Calle A, Valdivieso LR, Fava CM, Klein FR, Torralva T, Gleichgerrcht E, et al: Improvement in executive function after unilateral carotid artery stenting for severe asymptomatic stenosis. J Neurosurg. 116:179–184. 2012. View Article : Google Scholar
24	Phelps ME, Huang SC, Hoffman EJ, Selin C and Kuhl DE: Cerebral extraction of N-13 ammonia: Its dependence on cerebral blood flow and capillary permeability - surface area product. Stroke. 12:607–619. 1981. View Article : Google Scholar : PubMed/NCBI
25	Butterworth RF: Pathophysiology of hepatic encephalopathy: A new look at ammonia. Metab Brain Dis. 17:221–227. 2002. View Article : Google Scholar
26	Keiding S, Sørensen M, Bender D, Munk OL, Ott P and Vilstrup H: Brain metabolism of 13N-ammonia during acute hepatic encephalopathy in cirrhosis measured by positron emission tomography. Hepatology. 43:42–50. 2006. View Article : Google Scholar
27	Sørensen M, Munk OL and Keiding S: Backflux of ammonia from brain to blood in human subjects with and without hepatic encephalopathy. Metab Brain Dis. 24:237–242. 2009. View Article : Google Scholar