Advertisement
Original research| Volume 99, ISSUE 12, P2532-2539.e1, December 2018

Determining Peak Cough Flow Cutoff Values to Predict Aspiration Pneumonia Among Patients With Dysphagia Using the Citric Acid Reflexive Cough Test

      Highlights

      • Reflexive cough strength ≤59 L/min may indicate high risk of respiratory infection.
      • Peak cough flow cutoff value improves accuracy of aspiration pneumonia prediction.
      • Objective measurement of reflexive cough strength may predict aspiration pneumonia.

      Abstract

      Objective

      To investigate the clinical usefulness of the peak cough flow generated during the citric acid reflexive cough test (0.28 mol/L) by determining the appropriate cutoff values that could accurately predict aspiration pneumonia within the first 6 months after onset.

      Design

      Retrospective analysis of a prospectively maintained database.

      Setting

      University-affiliated hospital.

      Participants

      Patients (N=163) with first-ever diagnosed dysphagia attributable to cerebrovascular disease, who had undergone the citric acid reflexive cough test on the same day they underwent the instrumental assessment of swallowing, such as videofluoroscopy or the functional endoscopic swallowing test.

      Interventions

      Not applicable.

      Main Outcome Measures

      Peak cough flow (L/min) from the citric acid reflexive cough test.

      Results

      A final 163 patients had full medical records with 6-month follow-up. Receiver operating curve analysis showed that peak cough flow cutoff values set at 59 L/min were significantly associated with aspiration pneumonia (area under the curve [AUC] 95% confidence interval =0.88 [0.83-0.93]). This cutoff value significantly (P<.001) predicted the risk of aspiration pneumonia with an odds ratio of 21.56 (9.62-48.28). A multivariate regression logistic regression analysis model including initial dysphagia severity, low body mass index, and decreased level of cognition showed that inclusion of the peak cough flow from the citric acid reflexive cough test significantly improved the predictive model of aspiration pneumonia within the first 6 months after onset (AUC=0.91 vs 0.79).

      Conclusions

      Those with reflexive cough strength less than 59 L/min may be at high risk of respiratory infections within the first 6 months after dysphagia onset. Objective measurement of reflexive cough strength may help to predict those at risk of aspiration pneumonia.

      Keywords

      List of abbreviations:

      AUC (area under the curve), BMI (body mass index), FOIS (Functional Oral Intake Scale), GDS (Global Deterioration Scale), MMSE (Mini-Mental State Examination), mRS (modified Rankin scale), OR (odds ratio), PCF (peak cough flow), ROC (receiver operating characteristic)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Archives of Physical Medicine and Rehabilitation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Smith Hammond C.A.
        • Goldstein L.B.
        • Zajac D.J.
        • Gray L.
        • Davenport P.W.
        • Bolser D.C.
        Assessment of aspiration risk in stroke patients with quantification of voluntary cough.
        Neurology. 2001; 56: 502-506
        • Ward K.
        • Seymour J.
        • Steier J.
        • et al.
        Acute ischaemic hemispheric stroke is associated with impairment of reflex in addition to voluntary cough.
        Eur Respir J. 2010; 36: 1383-1390
        • Smith Hammond C.A.
        • Goldstein L.B.
        • Horner R.D.
        • et al.
        Predicting aspiration in patients with ischemic stroke: comparison of clinical signs and aerodynamic measures of voluntary cough.
        Chest. 2009; 135: 769-777
        • Daniels S.K.
        • Brailey K.
        • Priestly D.H.
        • Herrington L.R.
        • Weisberg L.A.
        • Foundas A.L.
        Aspiration in patients with acute stroke.
        Arch Phys Med Rehabil. 1998; 79: 14-19
        • Addington W.R.
        • Stephens R.E.
        • Widdicombe J.G.
        • Rekab K.
        Effect of stroke location on the laryngeal cough reflex and pneumonia risk.
        Cough. 2005; 1: 4
        • Hinchey J.A.
        • Shephard T.
        • Furie K.
        • Smith D.
        • Wang D.
        • Tonn S.
        Formal dysphagia screening protocols prevent pneumonia.
        Stroke. 2005; 36: 1972-1976
        • Ingeman A.
        • Andersen G.
        • Hundborg H.H.
        • Svendsen M.L.
        • Johnsen S.P.
        Processes of care and medical complications in patients with stroke.
        Stroke. 2011; 42: 167-172
        • Martino R.
        • Foley N.
        • Bhogal S.
        • Diamant N.
        • Speechley M.
        • Teasell R.
        Dysphagia after stroke: incidence, diagnosis, and pulmonary complications.
        Stroke. 2005; 36: 2756-2763
        • Bach J.R.
        • Saporito L.R.
        Criteria for extubation and tracheostomy tube removal for patients with ventilatory failure. A different approach to weaning.
        Chest. 1996; 110: 1566-1571
        • Widdicombe J.G.
        • Addington W.R.
        • Fontana G.A.
        • Stephens R.E.
        Voluntary and reflex cough and the expiration reflex; implications for aspiration after stroke.
        Pulm Pharmacol Ther. 2011; 24: 312-317
        • Vilardell N.
        • Rofes L.
        • Nascimento W.V.
        • Muriana D.
        • Palomeras E.
        • Clave P.
        Cough reflex attenuation and swallowing dysfunction in sub-acute post-stroke patients: prevalence, risk factors, and clinical outcome.
        Neurogastroenterol Motil. 2017; 29https://doi.org/10.1111/nmo.12910
        • Sato M.
        • Tohara H.
        • Iida T.
        • Wada S.
        • Inoue M.
        • Ueda K.
        Simplified cough test for screening silent aspiration.
        Arch Phys Med Rehabil. 2012; 93: 1982-1986
        • Miles A.
        • Huckabee M.L.
        Intra- and inter-rater reliability for judgement of cough following citric acid inhalation.
        Int J Speech Lang Pathol. 2013; 15: 209-215
        • Guillen-Sola A.
        • Chiarella S.C.
        • Martinez-Orfila J.
        • et al.
        Usefulness of citric cough test for screening of silent aspiration in subacute stroke patients: a prospective study.
        Arch Phys Med Rehabil. 2015; 96: 1277-1283
        • Wakasugi Y.
        • Tohara H.
        • Nakane A.
        • et al.
        Usefulness of a handheld nebulizer in cough test to screen for silent aspiration.
        Odontology. 2014; 102: 76-80
        • Addington W.R.
        • Stephens R.E.
        • Gilliland K.
        • Rodriguez M.
        Assessing the laryngeal cough reflex and the risk of developing pneumonia after stroke.
        Arch Phys Med Rehabil. 1999; 80: 150-154
        • Morice A.H.
        • Fontana G.A.
        • Belvisi M.G.
        • et al.
        ERS guidelines on the assessment of cough.
        Eur Respir J. 2007; 29: 1256-1276
        • Choi Y.M.
        • Park G.Y.
        • Yoo Y.
        • Sohn D.
        • Jang Y.
        • Im S.
        Reduced diaphragm excursion during reflexive citric acid cough test in subjects with subacute stroke.
        Respir Care. 2017; 62: 1571-1581
        • Chumbler N.R.
        • Williams L.S.
        • Wells C.K.
        • et al.
        Derivation and validation of a clinical system for predicting pneumonia in acute stroke.
        Neuroepidemiology. 2010; 34: 193-199
        • van der Maarel-Wierink C.D.
        • Vanobbergen J.N.
        • Bronkhorst E.M.
        • Schols J.M.
        • de Baat C.
        Meta-analysis of dysphagia and aspiration pneumonia in frail elders.
        J Dent Res. 2011; 90: 1398-1404
        • American Thoracic Society/European Respiratory Society
        ATS/ERS statement on respiratory muscle testing.
        Am J Respir Crit Care Med. 2002; 166: 518-624
        • Lee S.C.
        • Kang S.W.
        • Kim M.T.
        • Kim Y.K.
        • Chang W.H.
        • Im S.H.
        Correlation between voluntary cough and laryngeal cough reflex flows in patients with traumatic brain injury.
        Arch Phys Med Rehabil. 2013; 94: 1580-1583
        • Kulnik S.T.
        • Birring S.S.
        • Hodsoll J.
        • Moxham J.
        • Rafferty G.F.
        • Kalra L.
        Higher cough flow is associated with lower risk of pneumonia in acute stroke.
        Thorax. 2016; 71: 474-475
        • Miles A.
        • Moore S.
        • McFarlane M.
        • Lee F.
        • Allen J.
        • Huckabee M.L.
        Comparison of cough reflex test against instrumental assessment of aspiration.
        Physiol Behav. 2013; 118: 25-31
        • Mahoney F.I.
        • Barthel D.W.
        Functional evaluation: the Barthel index.
        Md State Med J. 1965; 14: 61-65
        • Berg K.
        • Wood-Dauphinee S.
        • Williams J.I.
        The balance scale: reliability assessment with elderly residents and patients with an acute stroke.
        Scand J Rehabil Med. 1995; 27: 27-36
        • Wade D.T.
        Measurement in neurological rehabilitation.
        Curr Opin Neurol Neurosurg. 1992; 5: 682-686
        • Folstein M.F.
        • Folstein S.E.
        • McHugh P.R.
        “Mini-mental state”. a practical method for grading the cognitive state of patients for the clinician.
        J Psychiatr Res. 1975; 12: 189-198
        • Reisberg B.
        • Ferris S.H.
        • de Leon M.J.
        • Crook T.
        The Global Deterioration Scale for assessment of primary degenerative dementia.
        Am J Psychiatry. 1982; 139: 1136-1139
        • Morice A.H.
        • Kastelik J.A.
        • Thompson R.
        Cough challenge in the assessment of cough reflex.
        Br J Clin Pharmacol. 2001; 52: 365-375
        • Stephens R.E.
        • Addington W.R.
        • Widdicombe J.G.
        Effect of acute unilateral middle cerebral artery infarcts on voluntary cough and the laryngeal cough reflex.
        Am J Phys Med Rehabil. 2003; 82: 379-383
        • Langmore S.E.
        • Terpenning M.S.
        • Schork A.
        • et al.
        Predictors of aspiration pneumonia: how important is dysphagia?.
        Dysphagia. 1998; 13: 69-81
        • Kojima A.
        • Imoto Y.
        • Osawa Y.
        • Fujieda S.
        Predictor of rehabilitation outcome for dysphagia.
        Auris Nasus Larynx. 2014; 41: 294-298
        • Matsumura T.
        • Mitani Y.
        • Oki Y.
        • Fujimoto Y.
        • Ishikawa A.
        Risk factors for the onset of aspiration pneumonia among stroke patients in the recovery stage.
        Nihon Ronen Igakkai Zasshi. 2014; 51: 364-368
        • Maeda K.
        • Akagi J.
        Muscle mass loss is a potential predictor of 90-day mortality in older adults with aspiration pneumonia.
        J Am Geriatr Soc. 2017; 65: e18-e22
        • Jodkowski J.S.
        • Berger A.J.
        Influences from laryngeal afferents on expiratory bulbospinal neurons and motoneurons.
        J Appl Physiol (1985). 1988; 64: 1337-1345
        • Bongianni F.
        • Corda M.
        • Fontana G.
        • Pantaleo T.
        Influences of superior laryngeal afferent stimulation on expiratory activity in cats.
        J Appl Physiol (1985). 1988; 65: 385-392

      References

        • Minnerup J.
        • Wersching H.
        • Brokinkel B.
        • et al.
        The impact of lesion location and lesion size on poststroke infection frequency.
        J Neurol Neurosurg Psychiatry. 2010; 81: 198-202
        • Garner J.S.
        • Jarvis W.R.
        • Emori T.G.
        • Horan T.C.
        • Hughes J.M.
        CDC definitions for nosocomial infections, 1988.
        Am J Infect Control. 1988; 16: 128-140
        • Walter U.
        • Knoblich R.
        • Steinhagen V.
        • Donat M.
        • Benecke R.
        • Kloth A.
        Predictors of pneumonia in acute stroke patients admitted to a neurological intensive care unit.
        J Neurol. 2007; 254: 1323-1329
        • Crary M.A.
        • Mann G.D.
        • Groher M.E.
        Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients.
        Arch Phys Med Rehabil. 2005; 86: 1516-1520
        • Rosenbek J.C.
        • Robbins J.A.
        • Roecker E.B.
        • Coyle J.L.
        • Wood J.L.
        A penetration-aspiration scale.
        Dysphagia. 1996; 11: 93-98