Skip to main content
SpringerLink
Log in

Hypocapnia Induced by Hyperventilation with Indocyanine Green Kinetics Detects the Effect of Staged Carotid Angioplasty to Avoid Hyperperfusion in Patients with Impaired Cerebral Hemodynamic Reserve

  • Original Article
  • Published:
Translational Stroke Research Aims and scope Submit manuscript

Abstract

Cerebral hyperperfusion syndrome (CHS) is a serious complication following carotid artery stenting (CAS). Staged angioplasty (AP) could potentially prevent CHS and hyperperfusion phenomenon (HPP) after revascularization. However, methods for measuring the effects of staged AP on cerebral hemodynamic reserve have not been established. Here, we evaluated whether indocyanine green kinetics and near-infrared spectroscopy (ICG-NIRS) with hypocapnia induced by hyperventilation can detect the effects of staged AP on hemodynamic reserve to prevent CHS after CAS. Participants comprised 44 patients at high risk of CHS, whose ipsilateral cerebrovascular reactivity (CVR) was impaired on preoperative single photon emission computed tomography (SPECT). Patients were divided into a staged AP group (n=13) and a regular CAS group (n=31). In the staged AP group, stenting was performed 3 weeks after staged AP. In the regular CAS group, 16 cases (52%) showed HPP, and five (16%) presented with CHS after CAS, while no HPP or CHS occurred in the staged AP group (p=0.001). Changes in blood flow index (BFI) and time to peak (TTP) ratio during hypocapnia calculated from ICG-NIRS indicated a significant linear relationship with preprocedural CVR on SPECT (r=−0.710, 0.632, respectively; p<0.0001 each). BFI and TTP ratios during hypocapnia were significantly improved after staged AP (p<0.001 each). Furthermore, significant linear correlations were observed between BFI and TTP ratio during hypocapnia and postoperative asymmetry index AI (r=0.405, −0.475, respectively; p<0.01 each). Hypocapnia induced by hyperventilation under ICG-NIRS appears useful for detecting the effects of staged AP on hemodynamic reserve in patients at high risk of CHS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The datasets analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Ogasawara K, Sakai N, Kuroiwa T, Hosoda K, Iihara K, Toyoda K, et al. Japanese society for treatment at neck in cerebrovascular disease study G: intracranial hemorrhage associated with cerebral hyperperfusion syndrome following carotid endarterectomy and carotid artery stenting: retrospective review of 4494 patients. J Neurosurg. 2007;107(6):1130–6.

    Article  Google Scholar 

  2. Yoshimura S, Kitajima H, Enomoto Y, Yamada K, Iwama T. Staged angioplasty for carotid artery stenosis to prevent postoperative hyperperfusion. Neurosurgery. 2009;64(3 Suppl):ons122–8. discussion ons128–129.

    PubMed  Google Scholar 

  3. Hayakawa M, Sugiu K, Yoshimura S, Hishikawa T, Yamagami H, Fukuda-Doi M, et al. Effectiveness of staged angioplasty for avoidance of cerebral hyperperfusion syndrome after carotid revascularization. J Neurosurg. 2019;18:1–11.

  4. Hosoda K, Kawaguchi T, Ishii K, Minoshima S, Shibata Y, Iwakura M, et al. Prediction of hyperperfusion after carotid endarterectomy by brain SPECT analysis with semiquantitative statistical mapping method. Stroke. 2003;34(5):1187–93.

    Article  Google Scholar 

  5. Al-Rawi PG, Kirkpatrick PJ. Tissue oxygen index: thresholds for cerebral ischemia using near-infrared spectroscopy. Stroke. 2006;37(11):2720–5.

    Article  Google Scholar 

  6. Germon TJ, Young AE, Manara AR, Nelson RJ. Extracerebral absorption of near infrared light influences the detection of increased cerebral oxygenation monitored by near infrared spectroscopy. J Neurol Neurosurg Psychiatry. 1995;58(4):477–9.

    Article  CAS  Google Scholar 

  7. Kuebler WM, Sckell A, Habler O, Kleen M, Kuhnle GE, Welte M, et al. Noninvasive measurement of regional cerebral blood flow by near-infrared spectroscopy and indocyanine green. J Cereb Blood Flow Metab. 1998;18(4):445–56.

    Article  CAS  Google Scholar 

  8. Terborg C, Bramer S, Harscher S, Simon M, Witte OW. Bedside assessment of cerebral perfusion reductions in patients with acute ischaemic stroke by near-infrared spectroscopy and indocyanine green. J Neurol Neurosurg Psychiatry. 2004;75(1):38–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Terborg C, Groschel K, Petrovitch A, Ringer T, Schnaudigel S, Witte OW, et al. Noninvasive assessment of cerebral perfusion and oxygenation in acute ischemic stroke by near-infrared spectroscopy. Eur Neurol. 2009;62(6):338–43.

    Article  CAS  Google Scholar 

  10. Nakagawa I, Park HS, Yokoyama S, Yamada S, Motoyama Y, Park YS, et al. Indocyanine green kinetics with near-infrared spectroscopy predicts cerebral hyperperfusion syndrome after carotid artery stenting. PLoS One. 2017;12(7):e0180684.

    Article  Google Scholar 

  11. Guven Yilmaz S, Palamar M, Gurgun C. Acute pulmonary oedema due to single dose acetazolamide taken after cataract surgery. BMJ Case Rep. 2016;11:bcr2016214829.

  12. Zimmermann S, Achenbach S, Wolf M, Janka R, Marwan M, Mahler V. Recurrent shock and pulmonary edema due to acetazolamide medication after cataract surgery. Heart Lung. 2014;43(2):124–6.

    Article  CAS  Google Scholar 

  13. Kobari M, Gotoh F, Fukuuchi Y, Tanaka K, Suzuki N, Uematsu D. Quantitative measurement of blood flow velocity in feline pial arteries during hemorrhagic hypotension and hypercapnia. Stroke. 1987;18(2):457–63.

    Article  CAS  Google Scholar 

  14. Nariai T, Senda M, Ishii K, Wakabayashi S, Yokota T, Toyama H, et al. Posthyperventilatory steal response in chronic cerebral hemodynamic stress: a positron emission tomography study. Stroke. 1998;29(7):1281–92.

    Article  CAS  Google Scholar 

  15. Nakagawa I, Yokoyama S, Wajima D, Nishimura F, Yamada S, Yokota H, et al. Hyperventilation and breath-holding test with indocyanine green kinetics predicts cerebral hyperperfusion after carotid artery stenting. J Cereb Blood Flow Metab. 2019;39(5):901–12.

    Article  CAS  Google Scholar 

  16. Yadav JS, Wholey MH, Kuntz RE, Fayad P, Katzen BT, Mishkel GJ, et al. Protected carotid-artery stenting versus endarterectomy in high-risk patients. N Engl J Med. 2004;351(15):1493–501.

    Article  CAS  Google Scholar 

  17. Hashikawa K, Matsumoto M, Moriwaki H, Oku N, Okazaki Y, Uehara T, et al. Split dose iodine-123-IMP SPECT: sequential quantitative regional cerebral blood flow change with pharmacological intervention. J Nucl Med. 1994;35(7):1226–33.

    CAS  PubMed  Google Scholar 

  18. Moriwaki H, Matsumoto M, Hashikawa K, Oku N, Ishida M, Seike Y, et al. Iodine-123-iomazenil and iodine-123-iodoamphetamine SPECT in major cerebral artery occlusive disease. J Nucl Med. 1998;39(8):1348–53.

    CAS  PubMed  Google Scholar 

  19. Matsumoto S, Nakahara I, Higashi T, Iwamuro Y, Watanabe Y, Takahashi K, et al. Near-infrared spectroscopy in carotid artery stenting predicts cerebral hyperperfusion syndrome. Neurology. 2009;72(17):1512–8.

    Article  CAS  Google Scholar 

  20. Mo D, Luo G, Wang B, Ma N, Gao F, Sun X, et al. Staged carotid artery angioplasty and stenting for patients with high-grade carotid stenosis with high risk of developing hyperperfusion injury: a retrospective analysis of 44 cases. Stroke Vasc Neurol. 2016;1(4):147–53.

    Article  Google Scholar 

  21. Murai S, Sugiu K, Hishikawa T, Hiramatsu M, Nishihiro S, Kidani N, et al. Safety and efficacy of staged angioplasty for patients at risk of hyperperfusion syndrome: a single-center retrospective study. Neuroradiology. 2020;62(4):503–10.

    Article  Google Scholar 

  22. Uchida K, Yoshimura S, Shirakawa M, Shindo S, Egashira Y, Iwama T, et al. Experience of Staged Angioplasty to Avoid Hyperperfusion Syndrome for Carotid Artery Stenosis. Neurol Med Chir. 2015;55(11):824–9.

    Article  Google Scholar 

  23. Mo D, Jia B, Shi H, Sun Y, Liu Q, Fan C, et al. Staged angioplasty versus regular carotid artery stenting in patients with carotid artery stenosis at high risk of hyperperfusion: a randomised clinical trial. Stroke Vasc Neurol. 2021;6(1):95–102.

  24. Wan Y, Wang H, Wang D, Tian H, Zuo J, Fang Q. The safety and efficacy of staged angioplasty for treating carotid stenosis with a high risk of hyperperfusion: A single-center retrospective study. Interv Neuroradiol. 2020;26(5):637–42.

    Article  Google Scholar 

  25. Nagashima H, Hongo K, Nagm A. Change in Cerebral Blood Flow after Palliative Percutaneous Angioplasty and Timing of Second Stage Carotid Artery Stenting in Staged Angioplasty. Neurol Med Chir. 2018;58(6):254–9.

    Article  Google Scholar 

  26. Kawai N, Hatakeyama T, Okauchi M, Kawanishi M, Shindo A, Kudomi N, et al. Cerebral blood flow and oxygen metabolism measurements using positron emission tomography on the first day after carotid artery stenting. J Stroke Cerebrovasc Dis. 2014;23(2):e55–64.

    Article  Google Scholar 

  27. Ogasawara K, Yukawa H, Kobayashi M, Mikami C, Konno H, Terasaki K, et al. Prediction and monitoring of cerebral hyperperfusion after carotid endarterectomy by using single-photon emission computerized tomography scanning. J Neurosurg. 2003;99(3):504–10.

    Article  Google Scholar 

  28. Buczek J, Karlinski M, Kobayashi A, Bialek P, Czlonkowska A. Hyperperfusion syndrome after carotid endarterectomy and carotid stenting. Cerebrovasc Dis. 2013;35(6):531–7.

    Article  Google Scholar 

  29. Gallerani M, Manzoli N, Fellin R, Simonato M, Orzincolo C. Anaphylactic shock and acute pulmonary edema after a single oral dose of acetazolamide. Am J Emerg Med. 2002;20(4):371–2.

    Article  Google Scholar 

  30. Al-Rawi PG, Smielewski P, Kirkpatrick PJ. Evaluation of a near-infrared spectrometer (NIRO 300) for the detection of intracranial oxygenation changes in the adult head. Stroke. 2001;32(11):2492–500.

    Article  CAS  Google Scholar 

  31. Park HS, Nakagawa I, Yokoyama S, Motoyama Y, Park YS, Wada T, et al. Amplitude of Tissue Oxygenation Index Change Predicts Cerebral Hyperperfusion Syndrome during Carotid Artery Stenting. World Neurosurg. 2017;9:548–555.

  32. Keller E, Nadler A, Alkadhi H, Kollias SS, Yonekawa Y, Niederer P. Noninvasive measurement of regional cerebral blood flow and regional cerebral blood volume by near-infrared spectroscopy and indocyanine green dye dilution. NeuroImage. 2003;20(2):828–39.

    Article  Google Scholar 

  33. Komoribayashi N, Ogasawara K, Kobayashi M, Saitoh H, Terasaki K, Inoue T, et al. Cerebral hyperperfusion after carotid endarterectomy is associated with preoperative hemodynamic impairment and intraoperative cerebral ischemia. J Cereb Blood Flow Metab. 2006;26(7):878–84.

    Article  Google Scholar 

  34. Piepgras DG, Morgan MK, Sundt TM Jr, Yanagihara T, Mussman LM. Intracerebral hemorrhage after carotid endarterectomy. J Neurosurg. 1988;68(4):532–6.

    Article  CAS  Google Scholar 

  35. Tajima Y, Takuwa H, Kokuryo D, Kawaguchi H, Seki C, Masamoto K, et al. Changes in cortical microvasculature during misery perfusion measured by two-photon laser scanning microscopy. J Cereb Blood Flow Metab. 2014;34(8):1363–72.

    Article  Google Scholar 

  36. Sato S, Kojima D, Shimada Y, Yoshida J, Fujimato K, Fujiwara S, et al. Preoperatively reduced cerebrovascular contractile reactivity to hypocapnia by hyperventilation is associated with cerebral hyperperfusion syndrome after arterial bypass surgery for adult patients with cerebral misery perfusion due to ischemic moyamoya disease. J Cereb Blood Flow Metab. 2018;38(6):1021–31.

    Article  Google Scholar 

  37. Wu F, Huang L, Lu G, Ge L, Zhang X, Cao W, et al. Two-Stage Cerebral Hemodynamic Changes in Staged Carotid Angioplasty and Stenting. J Stroke Cerebrovasc Dis. 2016;25(12):2814–20.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Nara Medical University, 840 Shijo-cho, Kashihara, Nara, 634-8522, Japan

    Ichiro Nakagawa, HunSoo Park, Masashi Kotsugi, Yasuhiro Takeshima, Ryosuke Matsuda, Shuichi Yamada, Young-Soo Park & Hiroyuki Nakase

  2. Department of Radiology, Nara Medical University, Nara, Japan

    Kaoru Myouchin

Authors
  1. Ichiro Nakagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. HunSoo Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masashi Kotsugi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kaoru Myouchin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yasuhiro Takeshima
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ryosuke Matsuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shuichi Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Young-Soo Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hiroyuki Nakase
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conception and design or analysis and interpretation of data, or both; IN, HP, MS. Drafting of the manuscript or revising it critically for important intellectual content; IN, HP, MS, KM, YT, RM, SY, YP, HN. Final approval of the manuscript submitted; IN, HN.

Corresponding author

Correspondence to Ichiro Nakagawa.

Ethics declarations

Ethics Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Conflicts of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nakagawa, I., Park, H., Kotsugi, M. et al. Hypocapnia Induced by Hyperventilation with Indocyanine Green Kinetics Detects the Effect of Staged Carotid Angioplasty to Avoid Hyperperfusion in Patients with Impaired Cerebral Hemodynamic Reserve. Transl. Stroke Res. 13, 77–87 (2022). https://doi.org/10.1007/s12975-021-00911-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12975-021-00911-7

Keywords

Search

Navigation