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Repeated Valsalva maneuvers promote symptomatic manifestations of cerebral microhemorrhages: implications for the pathogenesis of vascular cognitive impairment in older adults

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Abstract

Multifocal cerebral microhemorrhages (CMHs, also known as “cerebral microbleeds”), which are associated with rupture of small intracerebral vessels, have been recognized as an important cause for cognitive decline in older adults. Although recent studies demonstrate that CMHs are highly prevalent in patients 65 and older, many aspects of the pathogenesis and clinical significance of CMHs remain obscure. In this longitudinal observational study, a case of a 77-year-old man with multifocal CMHs is described, in whom the rupture of intracerebral vessels could be linked to repeatedly performing extended Valsalva maneuvers. This patient was initially seen with acute aphasia after performing a prolonged Valsalva maneuver during underwater swimming. T2-weighted magnetic resonance imaging revealed a left acute frontal intracerebral hemorrhage (ICH) with multiple CMHs. The aphasia was resolved and no cognitive impairment was present. Two years later, he developed unsteadiness and confusion after performing two prolonged Valsalva maneuvers during underwater swimming separated by about 12 days. Repeat brain imaging revealed an acute right and a subacute left ICH, with a marked interval increase in the number of CMHs. The patient also exhibited manifest memory loss after the second admission and was diagnosed with dementia. These observations suggest that prolonged Valsalva maneuver is potentially a common precipitating cause of both CMHs and symptomatic ICHs. The Valsalva maneuver both increases the systolic arterial pressure and gives rise to a venous pressure wave transmitted to the brain in the absence of the competent antireflux jugular vein valves. This pressure increase is superimposed on existing hypertension and/or increases in blood pressure due to exercise and increased venous return due to immersion of the body in water. We advocate that further studies are needed to distinguish between CMHs with arterial and venous origins and their potential to lead to ICH induced by Valsalva maneuver as well as to determine whether these lesions have a predilection for a particular location.

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Funding

This work was supported by grants from the American Heart Association (ST); the Oklahoma Center for the Advancement of Science and Technology (to AC, AY, and ZU); the National Center for Complementary and Alternative Medicine (R01-AT006526 to ZU); the National Institute on Aging (R01-AG055395, R01-AG047879, and R01-AG038747); the National Institute of Neurological Disorders and Stroke (NINDS; R01-NS100782 and R01-NS056218); a Pilot Grant from the Stephenson Cancer Center funded by the National Cancer Institute Cancer Center Support Grant P30CA225520 awarded to the University of Oklahoma Stephenson Cancer Center; the Oklahoma Shared Clinical and Translational Resources (OSCTR) program funded by the National Institute of General Medical Sciences (U54GM104938 to AY); the Presbyterian Health Foundation (to ZU, AC, AY, and CP); the European Union-funded grants EFOP-3.6.1-16-2016-00008, 20765-3/2018/FEKUTSTRAT, EFOP-3.6.2.-16-2017-00008, GINOP-2.3.2-15-2016-00048, and GINOP-2.3.3-15-2016-00032; the National Research, Development and Innovation Office (NKFI-FK123798); and the Hungarian Academy of Sciences (Bolyai Research Scholarship BO/00634/15 to PT). The authors acknowledge the support from the NIA-funded Geroscience Training Program in Oklahoma (T32AG052363).

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Authors and Affiliations

  1. Vascular Cognitive Impairment Program, Reynolds Oklahoma Center on Aging, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA

    Zoltan Ungvari, Andriy Yabluchanskiy, Stefano Tarantini, Peter Toth & Anna Csiszar

  2. Translational Geroscience Laboratory, Department of Geriatric Medicine, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA

    Zoltan Ungvari, Andriy Yabluchanskiy, Stefano Tarantini, Peter Toth & Anna Csiszar

  3. Institute for Translational Medicine, University of Pecs Medical School, Pecs, Hungary

    Zoltan Ungvari & Peter Toth

  4. Cerebrovascular Laboratory, Department of Neurosurgery and Szentagothai Research Center, University of Pecs Medical School, Pecs, Hungary

    Peter Toth

  5. Veterans Affairs Medical Center, Oklahoma City, OK, USA

    Angelia C. Kirkpatrick & Calin I. Prodan

  6. Department of Medicine, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA

    Angelia C. Kirkpatrick

  7. Department of Neurology, University of Oklahoma Health Sciences Center, 920 S. L. Young Blvd Suite 2040, Oklahoma City, 73104, OK, USA

    Calin I. Prodan

Authors
  1. Zoltan Ungvari
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  2. Andriy Yabluchanskiy
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  3. Stefano Tarantini
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  4. Peter Toth
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  5. Angelia C. Kirkpatrick
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  6. Anna Csiszar
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  7. Calin I. Prodan
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Corresponding author

Correspondence to Calin I. Prodan.

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Ungvari, Z., Yabluchanskiy, A., Tarantini, S. et al. Repeated Valsalva maneuvers promote symptomatic manifestations of cerebral microhemorrhages: implications for the pathogenesis of vascular cognitive impairment in older adults. GeroScience 40, 485–496 (2018). https://doi.org/10.1007/s11357-018-0044-9

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  • DOI: https://doi.org/10.1007/s11357-018-0044-9

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