Performance of questionnaires to predict sleep-disordered breathing in acute stroke patients
Martijn Petrus Josephus Dekkers
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Contribution: Conceptualization, Investigation, Writing - original draft, Methodology, Visualization, Formal analysis, Data curation, Writing - review & editing
Search for more papers by this authorCorresponding Author
Christian Michael Horvath
Department of Pulmonary Medicine, Allergology and Clinical Immunology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
Correspondence
Christian Michael Horvath, Universitätsklinik für Pneumologie, Allergologie und klinische Immunologie, Inselspital Bern, Universitätsspital Bern, Universität Bern, Freiburgstrasse 20, 3010 Bern, Switzerland.
Email: [email protected]
Contribution: Writing - original draft, Methodology, Writing - review & editing, Conceptualization
Search for more papers by this authorVanessa S. Woerz
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Contribution: Investigation, Writing - review & editing, Data curation
Search for more papers by this authorCorrado Bernasconi
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Interdisciplinary Sleep-Wake-Epilepsy-Center, Bern University Hospital (Inselspital) and University of Bern, Bern, Switzerland
Contribution: Writing - review & editing, Validation
Search for more papers by this authorSimone B. Duss
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Interdisciplinary Sleep-Wake-Epilepsy-Center, Bern University Hospital (Inselspital) and University of Bern, Bern, Switzerland
Contribution: Investigation, Writing - review & editing, Resources, Project administration
Search for more papers by this authorMarkus H. Schmidt
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Interdisciplinary Sleep-Wake-Epilepsy-Center, Bern University Hospital (Inselspital) and University of Bern, Bern, Switzerland
Contribution: Writing - review & editing, Validation, Supervision, Investigation
Search for more papers by this authorMauro Manconi
Neurocenter of Southern Switzerland, Ospedale Regionale di Lugano, Lugano, Switzerland
Contribution: Resources, Supervision, Writing - review & editing, Investigation
Search for more papers by this authorAnne-Kathrin Brill
Department of Pulmonary Medicine, Allergology and Clinical Immunology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
Interdisciplinary Sleep-Wake-Epilepsy-Center, Bern University Hospital (Inselspital) and University of Bern, Bern, Switzerland
Contribution: Writing - review & editing, Validation, Methodology
Search for more papers by this authorClaudio L. A. Bassetti
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Interdisciplinary Sleep-Wake-Epilepsy-Center, Bern University Hospital (Inselspital) and University of Bern, Bern, Switzerland
Department of Neurology, Sechenov First Moscow State Medical University, Moscow, Russia
Contribution: Resources, Supervision, Writing - review & editing, Funding acquisition, Investigation
Search for more papers by this authorMartijn Petrus Josephus Dekkers
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Contribution: Conceptualization, Investigation, Writing - original draft, Methodology, Visualization, Formal analysis, Data curation, Writing - review & editing
Search for more papers by this authorCorresponding Author
Christian Michael Horvath
Department of Pulmonary Medicine, Allergology and Clinical Immunology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
Correspondence
Christian Michael Horvath, Universitätsklinik für Pneumologie, Allergologie und klinische Immunologie, Inselspital Bern, Universitätsspital Bern, Universität Bern, Freiburgstrasse 20, 3010 Bern, Switzerland.
Email: [email protected]
Contribution: Writing - original draft, Methodology, Writing - review & editing, Conceptualization
Search for more papers by this authorVanessa S. Woerz
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Contribution: Investigation, Writing - review & editing, Data curation
Search for more papers by this authorCorrado Bernasconi
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Interdisciplinary Sleep-Wake-Epilepsy-Center, Bern University Hospital (Inselspital) and University of Bern, Bern, Switzerland
Contribution: Writing - review & editing, Validation
Search for more papers by this authorSimone B. Duss
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Interdisciplinary Sleep-Wake-Epilepsy-Center, Bern University Hospital (Inselspital) and University of Bern, Bern, Switzerland
Contribution: Investigation, Writing - review & editing, Resources, Project administration
Search for more papers by this authorMarkus H. Schmidt
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Interdisciplinary Sleep-Wake-Epilepsy-Center, Bern University Hospital (Inselspital) and University of Bern, Bern, Switzerland
Contribution: Writing - review & editing, Validation, Supervision, Investigation
Search for more papers by this authorMauro Manconi
Neurocenter of Southern Switzerland, Ospedale Regionale di Lugano, Lugano, Switzerland
Contribution: Resources, Supervision, Writing - review & editing, Investigation
Search for more papers by this authorAnne-Kathrin Brill
Department of Pulmonary Medicine, Allergology and Clinical Immunology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
Interdisciplinary Sleep-Wake-Epilepsy-Center, Bern University Hospital (Inselspital) and University of Bern, Bern, Switzerland
Contribution: Writing - review & editing, Validation, Methodology
Search for more papers by this authorClaudio L. A. Bassetti
Department of Neurology, Bern University Hospital (Inselspital) and University Bern, Bern, Switzerland
Interdisciplinary Sleep-Wake-Epilepsy-Center, Bern University Hospital (Inselspital) and University of Bern, Bern, Switzerland
Department of Neurology, Sechenov First Moscow State Medical University, Moscow, Russia
Contribution: Resources, Supervision, Writing - review & editing, Funding acquisition, Investigation
Search for more papers by this authorMartijn Petrus Josephus Dekkers, Christian Michael Horvath, Anne-Kathrin Brill and Claudio L.A. Bassetti contributed equally to this study.
Summary
Sleep-disordered breathing is common in stroke and may negatively affect its outcome. Screening for sleep-disordered breathing in this setting is of interest but poorly studied. We aimed to evaluate the performance of eight obstructive sleep apnea screening questionnaires to predict sleep-disordered breathing in acute stroke or transient ischaemic attack patients, and to assess the impact of stroke/transient ischaemic attack-specific factors on sleep-disordered breathing prediction. We analysed acute stroke/transient ischaemic attack patients (N = 195) from a prospective cohort (“Sleep Deficiency and Stroke Outcome study”). Assessments included anthropometrics, stroke-specific parameters, sleep history, an in-hospital respiratory polygraphy within the first week after stroke, and obstructive sleep apnea screening questionnaires (Berlin Questionnaire, Epworth Sleepiness Scale, STOP-BANG, NoSAS, Sleep Apnea Clinical Score, No-Apnea, Sleep Obstructive apnea score optimized for Stroke, SLEEP-IN). In a binary classification task for respiratory event index ≥ 15 per hr, we evaluated the performance of the above-mentioned questionnaires. We used logistic regression to identify predictors for sleep-disordered breathing in this cohort. The areas under the curve for respiratory event index ≥ 15 per hr were: Berlin Questionnaire 0.60; STOP-BANG 0.72; NoSAS 0.69; No-Apnea 0.69; Sleep Apnea Clinical Score 0.75; Epworth Sleepiness Scale 0.50; Sleep Obstructive apnea score optimized for Stroke 0.58; and SLEEP-IN 0.67. The No-Apnea had the lowest false omission rate (0.13), a sensitivity of 0.97 and a specificity of 0.12. In multiple logistic regression analysis (respiratory event index ≥ 15 per hr), age, neck circumference, National Institutes of Health Stroke Scale at admission, prior stroke, cardioembolic stroke aetiology and observed apneas were associated with sleep-disordered breathing. The logistic regression model performed similar (area under the curve 0.80) to Sleep Apnea Clinical Score (p = 0.402) and STOP-BANG (p = 0.127), but outperformed the other questionnaires. Neither existing questionnaires nor our statistical model are sufficient to accurately diagnose sleep-disordered breathing after stroke, thus requiring sleep study evaluation. The No-Apnea questionnaire may help to identify patients amenable to sleep testing.
CONFLICT OF INTEREST STATEMENT
The authors report no conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
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Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Arzt, M., Young, T., Peppard, P. E., Finn, L., Ryan, C. M., Bayley, M., & Bradley, T. D. (2010). Dissociation of obstructive sleep apnea from hypersomnolence and obesity in patients with stroke. Stroke, 41(3), e129–e134. https://doi.org/10.1161/STROKEAHA.109.566463
- Bassetti, C. L. A., Randerath, W., Vignatelli, L., Ferini-Strambi, L., Brill, A. K., Bonsignore, M. R., Grote, L., Jennum, P., Leys, D., Minnerup, J., Nobili, L., Tonia, T., Morgan, R., Kerry, J., Riha, R., McNicholas, W. T., & Papavasileiou, V. (2020). EAN/ERS/ESO/ESRS statement on the impact of sleep disorders on risk and outcome of stroke. European Journal of Neurology, 27(7), 1117–1136. https://doi.org/10.1111/ene.14201
- Berry, R. B., Brooks, R., Gamaldo, C., Harding, S. M., Lloyd, R. M., Quan, S. F., Troester, M. T., & Vaughn, B. V. (2017). AASM scoring manual updates for 2017 (version 2.4). Journal of Clinical Sleep Medicine, 13(5), 665–666. https://doi.org/10.5664/JCSM.6576
- Bonnin-Vilaplana, M., Arboix, A., Parra, O., García-Eroles, L., Montserrat, J. M., & Massons, J. (2009). Sleep-related breathing disorders in acute lacunar stroke. Journal of Neurology, 256(12), 2036–2042. https://doi.org/10.1007/s00415-009-5236-x
- Boulos, M. I., Elias, S., Wan, A., Im, J., Frankul, F., Atalla, M., Black, S. E., Basile, V. S., Sundaram, A., Hopyan, J. J., Boyle, K., Gladstone, D. J., Swartz, R. H., & Murray, B. J. (2017). Unattended hospital and home sleep apnea testing following cerebrovascular events. Journal of Stroke and Cerebrovascular Diseases, 26(1), 143–149. https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.09.001
- Boulos, M. I., Wan, A., Im, J., Elias, S., Frankul, F., Atalla, M., Black, S. E., Basile, V. S., Sundaram, A., Hopyan, J. J., Boyle, K., Gladstone, D. J., Murray, B. J., & Swartz, R. H. (2016). Identifying obstructive sleep apnea after stroke/TIA: Evaluating four simple screening tools. Sleep Medicine, 21, 133–139. https://doi.org/10.1016/j.sleep.2015.12.013
- Brown, D. L., He, K., Kim, S., Hsu, C.-W., Case, E., Chervin, R. D., & Lisabeth, L. D. (2020). Prediction of sleep-disordered breathing after stroke. Sleep Medicine, 75, 1–6. https://doi.org/10.1016/J.SLEEP.2020.05.004
- Brown, D. L., McDermott, M., Mowla, A., De Lott, L., Morgenstern, L. B., Kerber, K. A., Hegeman, G., Smith, M. A., Garcia, N. M., Chervin, R. D., & Lisabeth, L. D. (2014). Brainstem infarction and sleep-disordered breathing in the BASIC sleep apnea study. Sleep Medicine, 15(8), 887–891. https://doi.org/10.1016/j.sleep.2014.04.003
- Camilo, M. R., Sander, H. H., Eckeli, A. L., Fernandes, R. M. F., dos Santos-Pontelli, T. E. G., Leite, J. P., & Pontes-Neto, O. M. (2014). SOS score: An optimized score to screen acute stroke patients for obstructive sleep apnea. Sleep Medicine, 15(9), 1021–1024. https://doi.org/10.1016/j.sleep.2014.03.026
- Chen, R., Liu, W., Cheng, J., Zheng, Z., Ba, M., Peng, M., He, Q., Yang, H., Chen, T., & Hong, C. (2019). The No-apnea score vs. the other five questionnaires in screening for obstructive sleep apnea-hypopnea syndrome in patients with cerebral infarction. Journal of Thoracic Disease, 11(10), 4179–4187. https://doi.org/10.21037/jtd.2019.09.75
- Chung, F., Subramanyam, R., Liao, P., Sasaki, E., Shapiro, C., & Sun, Y. (2012). High STOP-bang score indicates a high probability of obstructive sleep apnoea. British Journal of Anaesthesia, 108(5), 768–775. https://doi.org/10.1093/bja/aes022
- DeLong, E. R., DeLong, D. M., & Clarke-Pearson, D. L. (1988). Comparing the areas under two or more correlated receiver operating characteristic curves: A nonparametric approach. Biometrics, 44(3), 837–845. http://www.ncbi.nlm.nih.gov/pubmed/3203132
- Duarte, R. L. M., Rabahi, M. F., Magalhães-da-Silveira, F. J., de Oliveira-E-Sá, T. S., Mello, F. C. Q., & Gozal, D. (2018). Simplifying the screening of obstructive sleep apnea with a 2-item model, No-apnea: A cross-sectional study. Journal of Clinical Sleep Medicine: JCSM, 14(7), 1097–1107. https://doi.org/10.5664/jcsm.7202
- Duss, S. B., Bauer-Gambelli, S. A., Bernasconi, C., Dekkers, M. P. J., Gorban-Peric, C., Kuen, D., Seiler, A., Oberholzer, M., Alexiev, F., Lippert, J., Brill, A.-K., Ott, S. R., Zubler, F., Horvath, T., Schmidt, M. H., Manconi, M., & Bassetti, C. L. A. (2023). Frequency and evolution of sleep-wake disturbances after ischemic stroke: A 2-year prospective study of 437 patients. Sleep Medicine, 101, 244–251. https://doi.org/10.1016/j.sleep.2022.10.007
- Epstein, L. J., Kristo, D., Strollo, P. J., Friedman, N., Malhotra, A., Patil, S. P., Ramar, K., Rogers, R., Schwab, R. J., Weaver, E. M., & Weinstein, M. D. (2009). Clinical guideline for the evaluation, management and long-term Care of Obstructive Sleep Apnea in adults. Journal of Clinical Sleep Medicine: JCSM, 5(3), 263–276. https://doi.org/10.5664/jcsm.27497
- Fisse, A. L., Kemmling, A., Teuber, A., Wersching, H., Young, P., Dittrich, R., Ritter, M., Dziewas, R., & Minnerup, J. (2017). The association of lesion location and sleep related breathing disorder in patients with acute ischemic stroke. PLoS One, 12(1), e0171243. https://doi.org/10.1371/journal.pone.0171243
- Flemons, W. W., Whitelaw, W. A., Brant, R., & Remmers, J. E. (1994). Likelihood ratios for a sleep apnea clinical prediction rule. American Journal of Respiratory and Critical Care Medicine, 150(5 I), 1279–1285. https://doi.org/10.1164/ajrccm.150.5.7952553
- Fu, S., Peng, X., Li, Y., Yang, L., & Yu, H. (2023). Effectiveness and feasibility of continuous positive airway pressure in patients with stroke and sleep apnea: A meta-analysis of randomized trials. Journal of Clinical Sleep Medicine: JCSM, 19(9), 1685–1696. https://doi.org/10.5664/JCSM.10680
- Hale, E., Gottlieb, E., Usseglio, J., & Shechter, A. (2023). Post-stroke sleep disturbance and recurrent cardiovascular and cerebrovascular events: A systematic review and meta-analysis. Sleep Medicine, 104, 29–41. https://doi.org/10.1016/J.SLEEP.2023.02.019
- Hasan, F., Gordon, C., Wu, D., Huang, H. C., Yuliana, L. T., Susatia, B., Marta, O. F. D., & Chiu, H. Y. (2021). Dynamic prevalence of sleep disorders following stroke or transient ischemic attack: Systematic review and meta-analysis. Stroke, 52(2), 655–663. https://doi.org/10.1161/STROKEAHA.120.029847
- Johns, M. W. (1991). A new method for measuring daytime sleepiness: The Epworth sleepiness scale. Sleep, 14(6), 540–545. http://www.ncbi.nlm.nih.gov/pubmed/1798888
- Kapur, V. K., Auckley, D. H., Chowdhuri, S., Kuhlmann, D. C., Mehra, R., Ramar, K., & Harrod, C. G. (2017). Clinical practice guideline for diagnostic testing for adult obstructive sleep apnea: An American Academy of sleep medicine clinical practice guideline. Journal of Clinical Sleep Medicine, 13(03), 479–504. https://doi.org/10.5664/jcsm.6506
- Lipford, M. C., Flemming, K. D., Calvin, A. D., Mandrekar, J., Brown, R. D., Somers, V. K., & Caples, S. M. (2015). Associations between cardioembolic stroke and obstructive sleep apnea. Sleep, 38(11), 1699–1705. https://doi.org/10.5665/sleep.5146
- Lisabeth, L. D., Sánchez, B. N., Lim, D., Chervin, R. D., Case, E., Morgenstern, L. B., Tower, S., & Brown, D. L. (2019). Sleep-disordered breathing and poststroke outcomes. Annals of Neurology, 86(2), 241–250. https://doi.org/10.1002/ANA.25515
- Love, B. B., & Bendixen, B. H. (1993). Classification of subtype of acute ischemic stroke definitions for use in a multicenter clinical trial. Stroke, 24(1), 35–41. https://doi.org/10.1161/01.STR.24.1.35
- Marti-Soler, H., Hirotsu, C., Marques-Vidal, P., Vollenweider, P., Waeber, G., Preisig, M., Tafti, M., Tufik, S. B., Bittencourt, L., Tufik, S., Haba-Rubio, J., & Heinzer, R., (2016). The NoSAS score for screening of sleep-disordered breathing: A derivation and validation study. The Lancet Respiratory Medicine, 4(9), 742–748. https://doi.org/10.1016/S2213-2600(16)30075-3
- Netzer, N. C., Stoohs, R. A., Netzer, C. M., Clark, K., & Strohl, K. P. (1999). Using the Berlin questionnaire to identify patients at risk for the sleep apnea syndrome. Annals of Internal Medicine, 172(1), ITC1–ITC14. https://doi.org/10.7326/AWED202001070
10.7326/AWED202001070 Google Scholar
- Ott, S. R., Fanfulla, F., Miano, S., Horvath, T., Seiler, A., Bernasconi, C., Cereda, C. W., Brill, A.-K., Young, P., Nobili, L., Manconi, M., & Bassetti, C. L. A. (2020). SAS care 1: Sleep-disordered breathing in acute stroke an transient ischaemic attack – Prevalence, evolution and association with functional outcome at 3 months, a prospective observational polysomnography study. ERJ Open Research, 6(2), 00334–02019. https://doi.org/10.1183/23120541.00334-2019
- Petrie, B. K., Sturzoiu, T., Shulman, J., Abbas, S., Masoud, H., Romero, J. R., Filina, T., Nguyen, T. N., Lau, H., Clark, J., Auerbach, S., Pyatkevich, Y. G., & Aparicio, H. J. (2021). Questionnaire and portable sleep test screening of sleep disordered breathing in acute stroke and TIA. Journal of Clinical Medicine, 10(16), 3568.
- Robin, X., Turck, N., Hainard, A., Tiberti, N., Lisacek, F., Sanchez, J.-C., & Müller, M. (2011). pROC: An open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics, 12(1), 77. https://doi.org/10.1186/1471-2105-12-77
- R Core Team (2022). R: A language and environment for statistical computing. R foundation for statistical computing. (n.d.). Retrieved December 22, 2022, from https://www.r-project.org/
- Rosen, I. M., Kirsch, D. B., Chervin, R. D., Carden, K. A., Ramar, K., Aurora, R. N., Kristo, D. A., Malhotra, R. K., Martin, J. L., Olson, E. J., Rosen, C. L., & Rowley, J. A. (2017). Clinical use of a home sleep apnea test: An American Academy of sleep medicine position statement. Journal of Clinical Sleep Medicine, 13(10), 1205–1207. https://doi.org/10.5664/jcsm.6774
- Seiler, A., Camilo, M., Korostovtseva, L., Haynes, A. G., Brill, A. K., Horvath, T., Egger, M., & Bassetti, C. L. (2019). Prevalence of sleep-disordered breathing after stroke and TIA: A meta-analysis. Neurology, 92(7), E648–E654. https://doi.org/10.1212/WNL.0000000000006904
- Sforza, E., Pichot, V., Martin, M. S., Barthélémy, J. C., & Roche, F. (2015). Prevalence and determinants of subjective sleepiness in healthy elderly with unrecognized obstructive sleep apnea. Sleep Medicine, 16(8), 981–986. https://doi.org/10.1016/j.sleep.2015.03.010
- Sico, J. J., Yaggi, H. K., Ofner, S., Concato, J., Austin, C., Ferguson, J., Qin, L., Tobias, L., Taylor, S., Vaz Fragoso, C. A., McLain, V., Williams, L. S., & Bravata, D. M. (2017). Development, validation, and assessment of an ischemic stroke or transient ischemic attack-specific prediction tool for obstructive sleep apnea. Journal of Stroke and Cerebrovascular Diseases, 26(8), 1745–1754. https://doi.org/10.1016/j.jstrokecerebrovasdis.2017.03.042
- Takala, M., Puustinen, J., Rauhala, E., & Holm, A. (2018). Pre-screening of sleep-disordered breathing after stroke: A systematic review. Brain and Behavior, 8(12), e01146. https://doi.org/10.1002/brb3.1146
- Toh, Z. A., Cheng, L. J., Wu, X. V., De Silva, D. A., Oh, H. X., Ng, S. X., He, H. G., & Pikkarainen, M. (2023). Positive airway pressure therapy for post-stroke sleep disordered breathing: A systematic review, meta-analysis and meta-regression. European Respiratory Review, 32(167), 220169. https://doi.org/10.1183/16000617.0169-2022
- Vat, S., Haba-Rubio, J., Tafti, M., Tobback, N., Andries, D., & Heinzer, R. (2015). Scoring criteria for portable monitor recordings: A comparison of four hypopnoea definitions in a population-based cohort. Thorax, 70, 1047–1053. https://doi.org/10.1136/thoraxjnl-2014-205982