Documenti di Didattica
Documenti di Professioni
Documenti di Cultura
discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/5258300
CITATIONS READS
36 361
10 authors, including:
All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Haruka Tohara
letting you access and read them immediately. Retrieved on: 16 April 2016
Dysphagia (2008) 23:364370
DOI 10.1007/s00455-008-9150-7
ORIGINAL ARTICLE
Abstract Many screening tests for dysphagia can be useful in screening for SA. Moreover, a screening system
given at bedside. However, they cannot accurately screen that included MWST and a cough test could accurately
for silent aspiration (SA). We studied the usefulness of a distinguish between the healthy who were safe in swal-
cough test to screen for SA and combined it with the lowing and SA patients who were unsafe.
modified water swallowing test (MWST) to make an
accurate screening system. Patients suspected of dysphagia Keywords Deglutition Deglutition disorders
(N = 204) were administered a cough test and underwent Screening test Silent aspiration Cough test
videofluorography (VF) or videoendoscopy (VE). Sensi-
tivity of the cough test for detection of SA was 0.87 with
specificity of 0.89. Of these 204 patients, 107 were also Videofluorography (VF) and videoendoscopy (VE) are
administered the MWST. Fifty-five were evaluated as considered the most accurate methods for the examination
normal by the screening system, 49 of whom were evalu- for dysphagia. However, many institutions lack the
ated as normal by VF or VE. Sixteen were evaluated as equipment required for these diagnostic tests. Thus, alter-
SA suspected by the screening system; seven of them native screening studies have been developed that easily
were normal, and seven were evaluated as having SA by can be performed at the patients bedside. The criteria for
VF or VE. Nineteen were evaluated as aspirating with many current screening tests include the presence of a
cough, 14 of whom had aspiration with cough as shown by cough [14]. Therefore, it is possible that diagnoses are
VF or VE. Seventeen were evaluated as having SA, 15 of missed in patients who show aspiration without cough
whom had SA shown by VF or VE. The cough test was (silent aspiration, SA) [5]. Furthermore, clinical bedside
assessment has been shown to miss up to 40% of dysphagia
patients with SA [6].
Y. Wakasugi (&) H. Tohara A. Nakane S. Goto
Y. Ouchi S. Mikushi S. Takeuchi H. Uematsu One study reported that SA was present in more than
Department of Gerodontology, Division of Gerontology and 70% of elderly patients with community-acquired pneu-
Gerodontology, Graduate School, Tokyo Medical and Dental monia [7]. SA can cause aspiration pneumonia in the elderly
University, 1-5-45, Yushima, Bunkyo, Tokyo 113-8549, Japan
[8]. Patients with laryngeal penetration, tracheobronchial
e-mail: wakasugi_y@yahoo.co.jp
aspiration, or silent tracheobronchial aspiration were
H. Tohara approximately 4 times, 10 times, and 13 times, respec-
Department of Dysphagia Rehabilitation, Nihon University, tively, more likely to develop pneumonia than those with
1-8-13, Surugadai, Kanda, Chiyoda, Tokyo 101-8310, Japan
normal swallowing [9]. There is no clear evidence that SA
F. Hattori relates to sensory loss. SA may relate to gradual desensiti-
National Hospital Organization, Tokyo National Hospital, 3-1-1, zation if aspiration is chronic [10]. SA has been reported to
Takeoka, Kiyose, Tokyo 204-8585, Japan occur in over 40% of patients referred for dysphagia eval-
uation in a rehabilitation hospital and in as many as 77% of
Y. Motohashi
Department of Dentistry, Musashimurayama Hospital, 1-1-5, ventilator-dependent patients [11]. Therefore, a screening
Enoki, Musashimurayama, Tokyo 208-0022, Japan test for SA is clinically valuable.
123
Y. Wakasugi et al.: Screening Test of Silent Aspiration 365
We studied the usefulness of a cough test to screen for patient was able to swallow but experienced dyspnea
SA. The cough test uses citric acid to detect SA. Because (difficulty breathing) after swallowing, a score of 2 was
the cough test looks at a patients cough rather than aspi- given. If the patient was able to swallow and experienced
ration, we then combined the cough test methods with coughing or wet-hoarseness after swallowing, a score of 3
other usual screening tests for aspiration and investigated was given. Otherwise, the patient was asked to perform two
whether the combined screening system could improve the dry (saliva) swallows. If the patient was able to swallow the
accuracy of dysphagia diagnosis. water but unable to perform either of the two dry swallows,
a score of 4 was recorded. If the patient was able to
complete the water and both dry swallows, a score of 5 was
Methods recorded. The entire procedure was repeated twice more
and the final score was defined as the lowest score on any
Participants in this study were 204 patients (131 men and trial.
73 women) who were suspected of having dysphagia and MWST was not conducted on patients clinically regar-
underwent VF or VE. They included both inpatients and ded as severe saliva aspirators. As a result, the number of
outpatients who had several clinical symptoms of dyspha- the patients receiving both screening tests was 107
gia such as coughing with eating, difficulty with eating, a (83 men and 24 women),with an average age of
fever or pneumonia by aspiration, and past history of suf- 69.23 13.09 years.
focation. None had a history of asthma. The average age All patients received VF (Medix-900DR, Hitachi Med-
was 69.90 11.70 years (mean SD) and ranged from ical Corp) or VE (Olympus ENF-P4) assessment of
18 to 100 years. The following preexisting conditions were swallowing to detect aspiration. VF was conducted fol-
found: 39% had cardiovascular disease (CVD), 24% head lowed by modified barium swallow (MBS) [18] and VE
or neck cancer, 17% neuromuscular disease, 15% respira- was followed by fiberoptic endoscopic evaluation of
tory disease, and 5% other diseases. This study received swallowing (FEES) [19]. The consistencies of the test
approval from the ethics committee of the faculty of den- foods used were thin liquid, thick liquid, cookies, and
tistry of the Tokyo Medical and Dental University. cornflakes. All the foods used in the VF included barium
Informed consent was obtained from all participants or sulfate. Thin and thick liquids were colored with green
their legal guardians. The study conformed to the Tokyo food dye for ease of visualization in the VE.
Medical and Dental University policies concerning
research on human subjects.
In the cough test, patients inhaled a mist of citric acid- Data Analysis
physiologic saline orally for 1 min with an ultrasonic
nebulizer. The inspector observed the number of times the Using the results of the VF or VE examination as the
patient coughed during the 1 min of nebulizing. More than standards, the sensitivity, specificity, efficiency, positive
five coughs was considered negative (normal), while less predictive value (PPV), and negative predictive value
than four coughs was regarded as positive [1214]. The (NPV) for SA detection were calculated. Then the results
concentration of citric acid was 1.0 w/v% [15]. Subjects of the screening system combining the cough test and the
were directed to breathe through the mouth mask because MWST were compared with the results of VF or VE.
inhaling through the mouth allows for a higher concen-
tration of inhaled particles than does inhaling through the
nose [16]. If patients had difficulty following these Results
instructions, a nose clip was applied to encourage the
patient to inhale orally. The ultrasonic nebulizer used was Results of the Cough Test
an OMRON NE-U17 with a particle size of 18 lm and
output rate greater than 3 ml/min. The cough test was The results of cough tests are shown in Table 1. There were
conducted on the day before, the same day, or the day after 97 patients who did not present with aspiration. Of these,
the VF or VE examination. 84 patients (86.6%) were negative and 13 patients (13.4%)
The cough test results were combined with the modified were positive. There were 37 patients who presented with
water swallowing test (MWST) for diagnosis [17]. Cold aspiration and cough. Of these, 36 patients (97.2%) were
water (3 ml) was placed on the floor of the mouth using a negative and one patient (2.8%) was positive. There were
5-ml syringe. Placement on the floor of the mouth pre- 18 patients who presented with aspiration without cough
vented premature spillage of test water into the pharynx. with a very little amount of aspiration (SA with a little
The patient was then instructed to swallow. If the patient aspiration). These patients coughed when there was a large
was unable to swallow, a score of 1 was given. If the amount of aspiration but did not cough with trace amounts
123
366 Y. Wakasugi et al.: Screening Test of Silent Aspiration
Table 1 Results of cough test included in the SA(-) analysis, sensitivity was 0.87,
VF/VE Cough test
specificity was 0.95, efficiency was 0.91, PPV was 0.94,
and NPV was 0.88 (Table 4). Likewise, if the SA with a
Negative Positive Total little aspiration group was included in the SA(+) analysis,
No aspiration 84 (86.6%) 13 (13.4%) 97 (47.5%) sensitivity was 0.67, specificity was 0.97, efficiency was
Aspiration with cough 36 (97.2%) 1 (2.8%) 37 (18.1%) 0.78, PPV was 0.98, and NPV was 0.61 (Table 5).
SA by little aspiration 16 (88.9%) 2 (11.1%) 18 (8.8%)
SA 7 (13.5%) 45 (86.5%) 52 (25.5%)
Results of the Cough Test and MWST
Total 143 (70.1%) 61 (29.9%) 204
Table 2 Screening of SA by cough test Table 4 Screening of SA by cough test in patients with aspiration
VF/VE Cough test VF/VE Cough test
Positive Negative Positive Negative
SA(+) 45 7 SA(+) 45 7
a a
SA(-) 16 136 SA(-) 3 52
Sensitivity = 0.87; specificity = 0.89; efficiency = 0.89; PPV = Sensitivity = 0.87; specificity = 0.95; efficiency = 0.91; PPV =
0.74; NPV = 0.95; N = 204 0.94; NPV = 0.8; N = 1078
a a
SA with a little aspiration was included in SA(-) SA with a little aspiration was included to SA(-)
Table 3 Screening of SA by cough test Table 5 Screening of SA by cough test in patients with aspiration
VF/VE Cough test VF/VE Cough test
Positive Negative Positive Negative
SA(+)a 47 23 SA(+)a 47 23
SA(-) 14 120 SA(-) 1 36
Sensitivity = 0.67; specificity = 0.90; efficiency = 0.82; PPV = Sensitivity = 0.67; specificity = 0.97; efficiency = 0.78; PPV =
0.77; NPV = 0.84; N = 204 0.98; NPV = 0.61; N = 107
a a
SA with a little aspiration was included in SA(+) SA with a little aspiration was included to SA (+)
123
Y. Wakasugi et al.: Screening Test of Silent Aspiration 367
123
368 Y. Wakasugi et al.: Screening Test of Silent Aspiration
acute stroke patients. They concluded that the cough test combined the oxygen saturation test and the 50-ml water-
was sufficient to assess the cough reflex and risk of aspi- swallowing test. Sensitivity and specificity of only oxygen
ration pneumonia in stroke patients. Sekizawa et al. [13] desaturation of 2% or more alone were 76.9% and 83.3%,
used the cough test to investigate whether weakness of the and those of the water-swallowing test alone were 84.6%
cough reflex was related to aspiration pneumonia. Patients and 75.0%. On the other hand, the combination of these
with aspiration pneumonia did not cough at the highest tests had 100% sensitivity and 70.8% specificity. Similarly,
concentration. Hammand et al. [48] analyzed the coughs of Tohara et al. [17] studied the accuracy of three nonvideo-
aspiration patients and healthy subjects. Objective analysis fluorographic (non-VFG) tests for assessing risk of
of the cough was sufficient to detect aspiration without aspiration: MWST and the food test (4 g of pudding) and
stress. Patients with an absent or weak cough reflex were at the X-ray test (static radiographs of the pharynx are taken
a higher risk of aspiration. They also assessed the cough before and after swallowing liquid barium). When MWST
reflex and aspiration of patients with acute CVA, and the was combined with the food test, sensitivity was 90% and
cough test showed a sensitivity of 68% and specificity of specificity was 56%. When all three non-VFG tests were
82%. Nakazawa et al. [49] determined that the thresholds combined, sensitivity was 90% and specificity was 71%.
of the cough test and swallow reflex induction test of We combined the MWST and the cough test because we
patients who developed pneumonia were higher than those wished to assess the swallowing reflex with the MWST and
of healthy subjects. Emergence of pneumonia was related assess the airway protective reflex with the cough test. We
to weaknesses in the airway protective reflex and swal- chose to use the MWST because it is safe, requires little
lowing ability. However, SA detection was not mentioned. volume, and its appropriateness was reported statistically.
Horner et al. [39] investigated the gag reflex, cough reflex, In our combination screening system of MWST and the
and swallowing reflex of acute stroke patients and found cough test, 89.1% of the predicted normal group were
that more than 60% of SA patients showed a weakened actually normal, 73.7% of the aspiration with cough group
cough response. were actually aspirators with cough, and 88.2% of the SA
In summary, the relationship of the cough test and group were actually silent aspirators. The confidence of the
aspiration or pneumonia has been reported in the past; combined screening system is thought to be clinically high.
however, these studies did not specifically attempt to detect Furthermore, the SA suspected group was actually half
SA. Furthermore, many of these studies demonstrated that normal and half SA. This demonstrates that if a patient is
a weak or absent cough response resulted in a higher risk of considered normal by the MWST but abnormal by the
aspiration pneumonia. cough test, it is possible that the patient is SA up to 50% of
The cough test is inexpensive and easy to perform, puts the time. The results of the combined screening system are
little stress on the patient, and enables a fast diagnosis of demonstrated in Figure 1.
swallowing difficulty. It can be performed on patients who When patients begin eating without VF or VE, we can
have difficulty following instructions, who are at high risk, distinguish healthy patients who are safe in swallowing
and who have low immunity. From the results of our study, from those who are SA who are not safe by using our
the cough test has good statistical reliability in the detec- combined screening system. In other words, healthy is
tion of SA. Therefore, the cough test is a useful SA normal with respect to both swallowing reflex and airway
screening tool. protective reflex and can perform the eating exercise or
start ingestion. Aspiration with cough is seen as abnor-
mal with respect to swallowing reflex but normal with
Usefulness of the Combined Screening System respect to the airway protective reflex, so these patients can
eat when the conditions are taken into account. SA is
The bedside examination has limitations in accurately abnormal for both reflexes, so they should not perform the
predicting or detecting the occurrence of aspiration. By eating exercise or start ingestion. SA suspected patients
combining tests that assess different important points have a normal swallowing reflex but an abnormal airway
clinically, the accuracy will increase [6]. Several studies protective reflex. SA and SA suspected patients need
have examined a combination of screening tests. Smith a further careful examination with VF or VE (Fig. 2). Of
et al. [50] combined oxygen saturation and standard bed- course, VF or VE should be done for patients with dys-
side swallowing assessments on 53 patients with acute phagia if the facility is well-equipped to do so. However, at
stroke confirmed by CT. Sensitivity and specificity of present, some patients do have opportunity to be evaluated
bedside swallowing assessment were only 80% and 68%, by VF or VE because of lack of proper equipment,
respectively, and those of O2 desaturation were only 87% accessibility, or other reasons. The screening tests dis-
and 39%. However, the combination of bedside assessment cussed here were inferior to VF and VE in accuracy, but we
and O2 desaturation were 73% and 76%. Lim et al. [6] still could obtain good statistical values for screening. It is
123
Y. Wakasugi et al.: Screening Test of Silent Aspiration 369
123
370 Y. Wakasugi et al.: Screening Test of Silent Aspiration
28. Collins MJ, Bakheit AMO. Does pulse oximetry reliably detect 43. Stephens RE, Addington WR, Widdicombe JG. Effect of acute
aspiration in dysphagic stroke patients? Stroke 1997;28:1773 unilateral middle cerebral artery infarcts on voluntary cough and
1775 the laryngeal cough reflex. Am J Phys Med Rehabil 2003;82:379
29. Sherman B, Nisenboum JM, Jesberqer BL, Morrow CA, Jes- 383
berqer JA. Assessment of dysphagia with the use of pulse 44. Addington WR, Stephens RE, Katherine G, Stuart M. Tartaric
oximetry. Dysphagia 1999;14:152156 acid-induced cough and the superior laryngeal nerve evoked
30. Sellars C, Dunnet C, Carter R. A preliminary comparison of potential. Am J Phys Med Rehabil 1998;77:523526
videofluoroscopy of swallow and pulse oximetry in the identifi- 45. Addington WR, Stephens RE, Katherine AG. Assessing the
cation of aspiration in dysphagic patients. Dysphagia laryngeal cough reflex and the risk of developing pneumonia
1998;13:8286 after stroke. an interhospital comparison. Stroke 1999;30:1203
31. Wang TG, Chang YC, Chen SY, Hsiao TY. Pulse oximetry does 1207
not reliably detect aspiration on videofluoroscopic swallowing 46. Addington WR, Stephens RE, Katherine G, Rodriguez M.
study. Arch Phys Med Rehabil 2005;86:730734 Assessing the laryngeal cough reflex and the risk of developing
32. Leder SB. Use of arterial oxygen saturation, heart rate, and blood pneumonia after stroke. Arch Phys Med Rehabil 1999;80:150
pressure as indirect objective physiologic markers to predict 154
aspiration. Dysphagia 2000;15:201205 47. Addington WR, Stephens RE, Ockey RR, Kann D, Rodriguez M.
33. Teramoto S, Fukuchi Y. Detection of aspiration and swallowing A new aspiration screening test to assess the need for a modified
disorder in older stroke patients: simple swallowing provocation barium swallow study. Arch Phys Med Rehabil 1995;76:1040,
test versus water swallowing test. Arch Phys Med Rehabil [abstract]
2000;81:15171519 48. Hammand CA, Goldstein LB, Zajac DJ, MD LG, Davenport
34. Aviv JE, Kim T, Sacco RL, Kaplan S, Goodhart K, Diamond B, PW, Bolser DC. Assessment of aspiration risk in stroke
Close LG. FEESST: a new bedside endoscopic test of the motor patients with quantification of voluntary cough. Neurology
and sensory components of swallowing. Ann Otol Rhinol Lar- 2001;56:502506
yngol 1998;107:378387 49. Nakazawa H, Sekizawa K, Ujiie Y, Sasaki H, Tokishima T. Risk
35. Zenner PM, Losinski DS, Mills RH. Using cervical auscultation of aspiration pneumonia in the elderly. Chest 1993;103:1636
in the clinical dysphagia examination in long term care. Dys- 1637
phagia 1998;2:127135 50. Smith HA, Lee SH, ONeill PA, Connolly MJ. The combination
36. Shaw JL, Sharpe S, Dyson SE, Pownall S, Walters S, Saul C, of bedside swallowing assessment and oxygen saturation moni-
Enderby P, Healy K, OSullivan H. Bronchial auscultation: an toring of swallowing in acute stroke: a safe and humane screening
effective adjunct to speech and language therapy bedside tool. Age Aging 2000;29:495499
assessment when detecting dysphagia and aspiration? Dysphagia
2004;19:211218
37. Oguchi K, Saitoh E, Mizuno M, Baba M, Okui M, Suzuki M. The Yoko Wakasugi DDS
repetitive saliva swallowing test (RSST) as a screening test of
functional dysphagia (1) normal values of RSST. Jpn J Rehabil Haruka Tohara DDS, PhD
Med 2000;37:383388, [in Japanese] Fumiko Hattori DDS, PhD
38. Splaingard ML, Hutchins B, Sulton LD, Chaudhuri G. Aspiration Yasutomo Motohashi DDS, PhD
in rehabilitation patients: videofluoroscopy vs bedside clinical
assessment. Arch Phys Med Rehabil 1988;69:637640 Ayako Nakane DDS, PhD
39. Horner J, Massey W. Silent aspiration following stroke. Neu- Shino Goto DDS, PhD
rology 1988;38:317319 Yukari Ouchi DDS
40. Stanners AJ. Clinical predictors of aspiration soon after stroke.
Age Aging 1993;2(Suppl 2):A47 Shinya Mikushi DDS
41. Linden P, Siebens AA. Dysphagia: predicting laryngeal pene- Syuhei Takeuchi DDS
tration. Arch Phys Med Rehabil 1983;64:281284 Hiroshi Uematsu DDS, PhD
42. Logemann JA, Veis S, Colangelo L. A screening procedure for
oropharyngeal dysphagia. Dysphagia 1999;14:4451
123