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      Increased microcirculatory heterogeneity in patients with obstructive sleep apnea

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          Abstract

          Introduction

          Obstructive sleep apnea (OSA) is the most common form of sleep disordered breathing and has been associated with major cardiovascular comorbidities. We hypothesized that the microcirculation is impaired in patients with OSA and that the magnitude of impairment correlates to OSA severity.

          Methods

          Subjects were consecutive patients scheduled for routine diagnostic polysomnography (PSG). OSA was defined by paradoxical rib cage movements together with abdominal excursions and by the apnea-hypopnea index (AHI) (events/hour; no apnea AHI<5; mild apnea 5≤AHI<15; moderate apnea 15≤AHI<30; severe apnea AHI ≥30). Sidestream darkfield imaging was used to assess the sublingual microcirculation. Recordings of sublingual microcirculation (5 random sites) were performed before and after overnight PSG. Data are summarized as mean (±SD); p values <0.05 were considered statistically significant.

          Results

          Thirty-three consecutive patients were included. OSA was diagnosed in 16 subjects (4 moderate, 12 severe). There was no significant difference in microcirculation between subjects with moderate OSA and without OSA. However, compared to subjects without OSA, subjects with severe OSA (AHI≥30) showed a significant decrease of microvascular flow index (-0.07±0.17 vs. 0.08±0.14; p = 0.02) and increase of microvascular flow index heterogeneity (0.06±0.15 vs. -0.06±0.11; p = 0.02) overnight. Multiple regression analysis (adjusted for age and gender) showed both decrease of flow and increase of flow heterogeneity associated with AHI (b = -0.41; F = 1.8; p = 0.04 and b = 0.43; F = 1.9; p = 0.03, respectively).

          Conclusion

          Acute overnight microcirculatory changes are observed in subjects with severe OSA characterized by decreased flow and increased flow heterogeneity.

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          Most cited references31

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          Sleep disordered breathing and mortality: eighteen-year follow-up of the Wisconsin sleep cohort.

          Terry Young, Laurel Ann Finn, Paul Peppard … (2008)
          Sleep-disordered breathing (SDB) is a treatable but markedly under-diagnosed condition of frequent breathing pauses during sleep. SDB is linked to incident cardiovascular disease, stroke, and other morbidity. However, the risk of mortality with untreated SDB, determined by polysomnography screening, in the general population has not been established. An 18-year mortality follow-up was conducted on the population-based Wisconsin Sleep Cohort sample (n = 1522), assessed at baseline for SDB with polysomnography, the clinical diagnostic standard. SDB was described by the number of apnea and hypopnea episodes/hour of sleep; cutpoints at 5, 15 and 30 identified mild, moderate, and severe SDB, respectively. Cox proportional hazards regression was used to estimate all-cause and cardiovascular mortality risks, adjusted for potential confounding factors, associated with SDB severity levels. All-cause mortality risk, adjusted for age, sex, BMI, and other factors was significantly increased with SDB severity. The adjusted hazard ratio (HR, 95% CI) for all-cause mortality with severe versus no SDB was 3.0 (1.4,6.3). After excluding persons who had used CPAP treatment (n = 126), the adjusted HR (95% CI) for all-cause mortality with severe versus no SDB was 3.8 (1.6,9.0); the adjusted HR (95% CI) for cardiovascular mortality was 5.2 (1.4,19.2). Results were unchanged after accounting for daytime sleepiness. Our findings of a significant, high mortality risk with untreated SDB, independent of age, sex, and BMI underscore the need for heightened clinical recognition and treatment of SDB, indicated by frequent episodes of apnea and hypopnea, irrespective of symptoms of sleepiness.
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            Sleep apnea as an independent risk factor for all-cause mortality: the Busselton Health Study.

            P. Liu, Carlos K. H. Wong, M Knuiman … (2008)
            Previously published cohort studies in clinical populations have suggested that obstructive sleep apnea (OSA) is a risk factor for mortality associated with cardiovascular disease. However, it is unknown whether sleep apnea is an independent risk factor for all-cause mortality in a community-based sample free from clinical referral bias. Residents of the Western Australian town of Busselton underwent investigation with a home sleep apnea monitoring device (MESAM IV). OSA was quantified via the respiratory disturbance index (RDI). Mortality status was determined in 397/400 participants (99.3%) after up to 14 years (mean follow-up 13.4 years) by data matching with the Australian National Death Index and the Western Australian Death Register. Univariate analyses and multivariate Cox proportional hazards modelling were used to ascertain the association between sleep apnea and mortality after adjustment for age, gender, body mass index, mean arterial pressure, total cholesterol, high-density lipoprotein cholesterol, diabetes, and medically diagnosed angina in those free from heart attack or stroke at baseline (n = 380). Among the 380 participants, 18 had moderate-severe OSA (RDI > or = 15/hr, 6 deaths) and 77 had mild OSA(RDI 5 to < 15/hr, 5 deaths). Moderate-to-severe OSA was independently associated with greater risk of all-cause mortality (fully adjusted hazard ratio [HR] = 6.24, 95% CL 2.01, 19.39) than non-OSA (n = 285, 22 deaths). Mild OSA (RDI 5 to < 15/hr) was not an independent risk factor for higher mortality (HR = 0.47, 95% CL 0.17, 1.29). Moderate-to-severe sleep apnea is independently associated with a large increased risk of all-cause mortality in this community-based sample.
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              Impairment of endothelium-dependent vasodilation of resistance vessels in patients with obstructive sleep apnea.

              B Phillips, P Thomson, V Accurso … (2000)
              Patients with obstructive sleep apnea (OSA) experience repetitive episodic hypoxemia with consequent sympathetic activation and marked blood pressure surges, each of which may impair endothelial function. We tested the hypothesis that patients with OSA have impaired endothelium-dependent vasodilation, even in the absence of overt cardiovascular disease. We studied 8 patients with OSA (age 44+/-4 years) and 9 obese control subjects (age 48+/-3 years). Patients with OSA were newly diagnosed, never treated for OSA, on no medications, and free of any other known diseases. All obese control subjects underwent complete overnight polysomnographic studies to exclude occult OSA. Resistance-vessel function was tested by use of forearm blood flow responses to intra-arterial infusions of acetylcholine (a vasodilator that stimulates endothelial release of nitric oxide), sodium nitroprusside (an exogenous nitric oxide donor), and verapamil (a calcium channel blocker). Conduit-vessel function was also evaluated by ultrasonography. Brachial artery diameter was measured under baseline conditions, during reactive hyperemia (with flow increase causing endothelium-dependent dilatation), and after sublingual administration of nitroglycerin (an endothelium-independent vasodilator). Patients with OSA had a blunted vasodilation in response to acetylcholine (P:<0.007), but responses to sodium nitroprusside and verapamil were not significantly different from those of control subjects. No significant difference in conduit-vessel dilation was evident between OSA patients and obese control subjects. Patients with OSA have an impairment of resistance-vessel endothelium-dependent vasodilation. This may be implicated in the pathogenesis of hypertension and heart failure in this condition.
              Article 0 comments Cited 105 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Lukas Ruzek: Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Karolina Svobodova: Role: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Lyle J. Olson: Role: MethodologyRole: Project administrationRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Ondrej Ludka: Role: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Ivan Cundrle Jr.:
                ORCID: http://orcid.org/0000-0002-7709-8021
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Andrea Romigi: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 1 September 2017
                Publication date Collection: 2017
                Volume: 12
                Issue: 9
                Electronic Location Identifier: e0184291
                Affiliations
                [1 ] Department of Anaesthesiology and Intensive Care, St. Anna's University Hospital Brno, Brno, Czech Republic
                [2 ] International Clinical Research Center, St. Anna's University Hospital Brno, Brno, Czech Republic
                [3 ] Faculty of Medicine, Masaryk University, Brno, Czech Republic
                [4 ] Division of Cardiovascular Diseases, Mayo Clinic, Rochester, Minnesota, United States of America
                [5 ] Internal Cardiology Department, University Hospital Brno, Brno, Czech Republic
                University of Rome Tor Vergata, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-7709-8021
                Article
                Publisher ID: PONE-D-17-12745
                DOI: 10.1371/journal.pone.0184291
                PMC ID: 5581006
                PubMed ID: 28863183
                SO-VID: dcfe1d9f-f61a-49ef-a136-eb4cf6c803c1
                Copyright © © 2017 Ruzek et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 1 April 2017
                Date accepted : 20 August 2017
                Page count
                Figures: 1, Tables: 3, Pages: 10
                Funding
                Funded by: National Program of Sustainability II (MEYS CR)
                Award ID: no. LQ1605
                Funded by: FNUSA-ICRC
                Award ID: CZ.1.05/1.1.00/02.0123
                This work was supported by the project no. LQ1605 from the National Program of Sustainability II (MEYS CR) and by the project FNUSA-ICRC no. CZ.1.05/1.1.00/02.0123 (OP VaVpI). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Medicine and Health Sciences
                Subject: Pulmonology
                Subject: Apnea
                Subject: Sleep Apnea
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Sleep Disorders
                Subject: Sleep Apnea
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Cardiovascular Physiology
                Subject: Blood Circulation
                Subject: Microcirculation
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Cardiovascular Physiology
                Subject: Blood Circulation
                Subject: Microcirculation
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Physiological Processes
                Subject: Sleep
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Physiological Processes
                Subject: Sleep
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Sleep Disorders
                Subject: Medicine and Health Sciences
                Subject: Clinical Medicine
                Subject: Clinical Neurophysiology
                Subject: Polysomnography
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Cardiovascular Anatomy
                Subject: Blood Vessels
                Subject: Capillaries
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Cardiovascular Anatomy
                Subject: Blood Vessels
                Subject: Capillaries
                Subject: Research and Analysis Methods
                Subject: Database and Informatics Methods
                Subject: Bioinformatics
                Subject: Sequence Analysis
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Physiological Processes
                Subject: Respiration
                Subject: Breathing
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Physiological Processes
                Subject: Respiration
                Subject: Breathing
                Custom metadata
                Data Availability All relevant data are within the paper and its Supporting Information files.

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