Authors:

Carlo Bianchi, MD
Paola Baiardi, PhD Pulmonary
Sonia Khirani, PhD
Giovanna Cantarella, MD

Affiliations:
From the Rehabilitation Unit, ORIGINAL RESEARCH ARTICLE
Fondazione Don Carlo Gnocchi, Centro
IRCCS BSanta Maria Nascente,[ Milan
(CB); Consorzio Valutazioni Biologiche
e Farmacologiche, Pavia (PB);
Department of Bronchopneumology, Cough Peak Flow as a Predictor of
Fondazione IRCCS Ca’ Granda
Ospedale Maggiore Policlinico, Milan
(SK); and Department of
Pulmonary Morbidity in Patients with
Otolaryngology, Fondazione IRCCS Ca’
Granda Ospedale Maggiore Policlinico,
Dysphagia
Milan, Italy (GC).

Correspondence:
All correspondence and requests for
reprints should be addressed to:
Giovanna Cantarella, MD, Department
of Otolaryngology, Fondazione IRCCS
Ca_ Granda Ospedale Maggiore
Policlinico, Via F. Sforza 35, 20122
Milano, Italy.
Disclosures:
Financial disclosure statements have
been obtained, and no conflicts of
interest have been reported by the
authors or by any individuals in control
of the content of this article.
0894-9115/12/9106-0000/0
American Journal of Physical
Medicine & Rehabilitation
Copyright * 2012 by Lippincott
Williams & Wilkins
DOI: 10.1097/PHM.0b013e3182556701
ABSTRACT
Bianchi C, Baiardi P, Khirani S, Cantarella G: Cough peak flow as a predictor of
pulmonary morbidity in patients with dysphagia. Am J Phys Med Rehabil
2012;91:00Y00.
Objective: The aim of this study was to ascertain whether an objective cough
measure relates to the risk of pulmonary complications in dysphagic patients with
persistent tracheobronchial aspiration.
Design: This is a retrospective observational study involving 55 dysphagic
patients who underwent a modified barium swallow study and pulmonary function
tests including cough peak flow measurement. The results were compared be-
tween subjects with and without pulmonary complications because of aspiration.
Results: The 18 patients (33%) with pulmonary complications had signifi-
cantly lower mean cough peak flow values (202.2 T 68.8 vs. 303.9 T 80.7 liters/
min; P G 0.001) than those without pulmonary complications. The finding of
tracheobronchial coating in a modified barium swallow was not related to the
occurrence of pulmonary morbidity. Receiver operating characteristic curve
analysis showed that a CPF level lower than 242 liters/min predicted the devel-
opment of pulmonary complications with a sensitivity of 77% and a specificity of
83%; the positive and negative predictive values were 65% and 90%,
respectively.
Conclusions: Our findings indicate that cough peak flow is a valuable pre-
dictor of respiratory prognosis in chronic aspiration. This finding suggests a new
rehabilitation strategy aimed at improving cough flows for dysphagic patients.
Key Words: Aspiration, Deglutition, Deglutition Disorders, Voluntary Cough, Aspiration
Pneumonia, Respiratory Prognosis, Cough Efficacy

www.ajpmr.com Pulmonary Morbidity in Patients with Dysphagia 1

Copyright © 2012 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

O ropharyngeal dysphagia can lead to severe
medical consequences, including pulmonary com-
plications. Common symptoms include coughing
and choking at mealtimes. Cough is a potential in-
dicator of the tracheobronchial aspiration of liquids
and/or solids, although Bsilent[ aspiration can also
occur in the absence of cough in some cases.1
The assessment of dysphagia is based on clin-
ical and instrumental examinations.2Y4 A video-
fluoroscopy swallowing study, also called a modified
barium swallow (MBS) study, is widely used and is
considered the gold standard for evaluating swal-
lowing safety.5 MBS allows for the assessment of
oral, pharyngeal, and esophageal swallowing patho-
physiology by changing the basic routine examina-
tion into a tailored one6 and is considered a useful
means of identifying and assessing aspiration risk.7
Nevertheless, it has been found that a videofluoro-
scopic finding of bolus penetration up to or below
the true vocal folds does not necessarily correlate
with the development of aspiration pneumonia,8,9
although a number of studies have shown a rela-
tionship between pneumonia and oropharyngeal
dysphagia, causing the aspiration of food.1
It has been suggested that the efficiency of
the laryngeal cough reflex explains the variability
in the occurrence of pulmonary complications in
patients with documented aspiration.5 It is known
that coughing is the main reflex mechanism pro-
tecting the respiratory apparatus from the aspira-
tion of foreign bodies in the case of swallowing
disorders,10 and it has also been stated that the
importance of coughing may lie in its voluntary
mechanism, if effectively used to clear secretions
from the airways.11 It has been shown that a cough
peak flow (CPF, a quantitative measure of cough
efficacy) of 160 liters/min is the minimum re-
quirement to clear airway debris for successful
extubation and that at least 270 liters/min is re-
quired to prevent the development of pulmonary
complications during intercurrent upper respira-
tory tract infections.12
Based on these previous findings, we designed
this study to clarify the role of cough effectiveness
in preventing the development of aspiration pneu-
monia in chronic aspiration. To this end, quantita-
tive cough measurements were made and correlated
with the clinical history of aspiration-related pul-
monary complications in a group of dysphagic pa-
tients with chronic aspiration. We hypothesized
that CPFs greater than 270 liters/min would sig-
nificantly decrease the risk of pulmonary compli-
cations in subjects with dysphagia.
2 Bianchi et al.
Copyright © 2012 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
METHODS
Study Design and Population
This is a retrospective observational study
considering a population of dysphagic patients se-
lected from more than 200 consecutive adults who
were referred to our swallowing center in a reha-
bilitation facility during a period of 15 years. The
inclusion criteria were as follows: dysphagia caused
by neurologic or iatrogenic causes (head and neck
surgery), persistent evidence of laryngeal penetra-
tion or tracheobronchial aspiration of a liquid and/
or solid bolus during MBS (a score of 95 on the 8-
point penetration/aspiration scale of Rosenbek
et al.13) despite swallowing therapy, and an ability
to cooperate during the clinical and instrumental
evaluation. The baseline presence of a percutaneous
gastrostomy (PEG) was not considered to be an
exclusion criterion if the patients had already begun
oral feeding or a swallowing rehabilitation program;
these patients were allowed to maintain or switch to
oral feeding if they had a satisfactory CPF. The study
was approved by our institutional review board, and
all of the patients signed an informed consent form.
Clinical History and Swallowing
Evaluation
The enrolled patients’ pulmonary clinical his-
tories were recorded from the time of the onset of
dysphagia to the time of their referral to the reha-
bilitation facility. The patients were considered to be
affected by pulmonary complications if they repor-
ted recurring (more than two episodes) bronchitis,
necessitating repeated antibiotic therapy or single
or recurring pneumonia (defined based on clinical
documentation and/or hospitalization). Continuous
nonfebrile airway secretions (defined as recurrent
daily cough and sputum production) were consid-
ered minor complications.
The patients were divided into two groups
based on their pulmonary clinical history: in group
1, there was evidence of major pulmonary compli-
cations, whereas in group 2, no pulmonary dis-
orders or only minor complications were evident.
MBS Study
The MBS study was performed with the patient
in a sitting position to allow a lateral view, using an
oral intake of liquid contrast medium (CM) followed
by a barium paste-impregnated food substance.
Episodes of laryngeal penetration and/or tra-
cheobronchial aspiration were defined according to
Logemann.5 Both were recorded for the liquid and/
or solid CM bolus and were rated using the 8-point
Am. J. Phys. Med. Rehabil. & Vol. 91, No. 6, June 2012
penetration/aspiration scale of Rosenbek et al.13 To
TABLE 1 Characteristics of the 55 dysphagic
determine the severity of the tracheobronchial as- subjects under study
piration more precisely, the MBS study was follo-
wed by a frontal chest x-ray to reveal the depth of Mean T SD
any occurrence of tracheobronchial coating of CM Characteristics or n (%)
(bronchogram), which was classified using a semi- Age, yrs 67.4 T 11.7
quantitative 5-point scale based on the extension Sex (male/female) 44 (80)/11 (20)
Diagnosis
of the tracheobronchial tree coating: 0, laryngeal
Stroke 23 (42)
penetration and/or tracheal coating without bron- Other neurologic disturbances 5 (9)
chial coating; 1, mild unilateral proximal bronchial Sequelae of skull base surgery 11 (20)
coating; 2, mild bilateral proximal bronchial coat- Sequelae of oro-pharyngo-laryn 16 (29)
geal surgery
ing; 3, diffuse monolateral bronchial coating; and 4, Paralysis (yes/no) 17 (31)/38 (69)
diffuse bilateral bronchial coating. The presence or Tetraplegia 8 (15)
absence of a cough reflex was recorded during the Diplegia 1 (2)
Hemiplegia 8 (15)
videofluoroscopic evaluation of CM penetration or Disease duration, mos 4 (1Y36; 4)a
aspiration.14 Silent aspiration was defined as the Follow-up, mos 12(4Y144; 9)a
entry of CM into the trachea or bronchial tree a
Median value (range; interquartile range).
without any associated cough reflex.

Pulmonary Function Tests

During the first evaluation, vital capacity and
peak expiratory flow were measured using a por-
table spirometer (Spirolab; Medical International
Research Company, Roma, Italy). Oxyhemoglobin
saturation (SpO2) was measured using an oximeter
(Nonin Medical Inc., Plymouth, MN), and end-tidal
CO2 tension (EtCO2) was measured using a cap-
nograph (Microcap; Oridion Medical 1987 Ltd.,
Jerusalem, Israel).
Cough Measurement
Cough effectiveness, expressed as CPF, was
assessed using a portable peak flow meter (Health
Scan Products Inc., Cedar Grove, NJ) during the
first visit. The sitting patients were asked to cough
forcefully into an oro-nasal mask that was connec-
ted to the peak flow meter. The maximum CPF in
five attempts was considered.
Statistical Analysis
The data are expressed as mean values T stan-
dard deviation in the case of normally distributed
continuous variables and frequencies in the case of
nominal variables. The continuous variables whose
distribution was far from normal (time since onset
of dysphagia and follow-up, see Table 1) are sum-
marized as median values and the interquartile
range (defined as the difference between the 75th
and 25th percentiles). The subjects with and with-
out pulmonary complications were compared using
an unpaired Student’s t test for the continuous
variables and the W2 test for the nominal variables.
Receiver operating characteristic curve analysis
was used to identify the threshold CPF value capable
of distinguishing patients with and without pul-
monary morbidity with the greatest sensitivity and
specificity, and its positive and negative predictive
values were calculated. The area under the receiver
operating characteristic curve was determined with
its 95% confidence intervals; values close to 1 in-
dicated the good discriminating power of CPF.
Data were analyzed using SPSS, Italian version
18 (SPSS for Windows, Rel. 18.0.0. 2009, SPSS Inc.,
Chicago, IL). A P value less than 0.05 was consid-
ered significant.
RESULTS
Fifty-five consecutive patients met the inclu-
sion criteria. Their characteristics are shown in
Table 1: 23 were affected by sequelae of stroke; 5 had
other neurologic disturbances; and 11 were affected
by sequelae of skull base surgery. In the remaining
16, dysphagia was caused by the sequelae of onco-
logic upper airway surgery (six reconstructive lar-
yngectomies, five supraglottic laryngectomies, and
five surgeries for oropharyngeal resection).
The median time from the onset of dysphagia to
referral to the rehabilitation service was 4 mos
(interquartile range, 4), and the median follow-up
time was 12 mos (interquartile range, 9). Fifteen
were smokers (27%), and all but one had undergone
upper airway surgery.
Eighteen (33%) patients had dysphagia-related
pulmonary complications (Group 1): 10 with bron-
chitis alone, 1 with pneumonia alone, and 7 with
both. Group 2 consisted of the 37 patients (67%)
without pulmonary complications. Irregular or fre-
quent airway secretions were present in 17 (94%)

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Copyright © 2012 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
 of the patients in group 1 and in 19 (51%) of the
patients in group 2 (P = 0.002). There was no be-
tween-group difference in terms of age (64.9 T 12.3
vs. 68.6 T 11.4 yrs; P = 0.28).
The MBS study (Table 2) documented liquid
aspiration in 53 patients (96%), solid aspiration in
46 (83%), and both liquids and solids were aspirated
in 44 (80%). None of the patients showed laryngeal
penetration alone. Chest x-ray demonstrated a
bronchogram caused by aspiration in 42 patients
(76%): 16 from group 1 (89%) and 26 (70%) from
group 2. Of the 13 patients with no bronchogram,
only two had pulmonary complications (15%). The
occurrence of a bronchogram was not statistically
related to the development of pulmonary compli-
cations (P = 0.13); furthermore, the depth of the
bronchogram defined by the 5-point semiquantita-
tive scale did not correlate with pulmonary mor-
bidity (P = 0.89). During the MBS study, there was
no cough reflex in seven group 1 patients (39%) and
seven group 2 patients (19%); the between-group
difference was not significant (P = 0.11).
Table 3 shows the results of the pulmonary
function tests. The patients in group 1 (with pul-
monary complications) had significantly lower CPF
levels (202.2 T 68.8 vs. 303.9 T 80.7 liters/min; P G
0.001) than did patients without pulmonary com-
plications. Lower vital capacity and SpO2 values
were also observed in group 1, whereas the per-
centage of predicted peak expiratory flow was not
different between the two groups.
The receiver operating characteristic curve
analysis estimated an area under the curve of 0.85
(95% CI, 0.74Y0.96), thus indicating that CPF was
capable of distinguishing subjects with and without
pulmonary complications. The best discriminatory
threshold was 242 liters/min, which had a sensi-
tivity of 77% and a specificity of 83%; the positive
and negative predictive values were 65% and 90%,
respectively. Of the 23 patients with a CPF less than
242 liters/min, 7 (30%) did not develop pulmonary
disorders; of the 32 patients with a CPF greater than
TABLE 2 Results of the modified barium swallow
study in the two groups of patients
Total Group 1 Group 2
(N = 55) (n = 18) (n = 37)
Aspiration for 53 (96%) 17 (94%) 36 (97%)
liquids
Aspiration for 46 (83%) 16 (89%) 30 (81%)
solids
Tracheobronchial 42 (76%) 16 (89%) 26 (70%)
coating
4 Bianchi et al.
Copyright © 2012 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
TABLE 3 Baseline respiratory variables in the
patients with and without pulmonary
complications (groups 1 and 2)
Group 1 Group 2
Variables (n = 18) (n = 37) P
CPF, liters/min 202.2 T 68.8 303.9 T 80.7 G0.001
VC, liters 2.36 T 0.91 3.05 T 0.94 0.03
VC% 64.1 T 25.9 85.1 T 14.6 0.01
PEF, liters/min 228.8 T 138.4 282.0 T 86.2 ns
PEF% 60.3 T 31.2 64.8 T 17.7 ns
SpO2, % 94.4 T 1.9 95.8 T 1.6 0.01
CPF, cough peak flow; VC, vital capacity; VC%, vital ca-
pacity expressed as percentage of predicted value; PEF, peak
expiratory flow; PEF%, peak expiratory flow expressed as
percentage of predicted value; SpO2, oxyhemoglobin satura-
tion; ns, not significant.
242 liters/min, 2 (6.2%) developed pulmonary
disorders.
Forty-one (74%) patients were oral feeders
before they were referred to our rehabilitation ser-
vice; of the 14 PEG feeders (26%), 3 had tracheos-
tomy tubes. None of the oral feeders underwent
PEG feeding after entering the study. Based on their
satisfactory CPF, PEG feeding was discontinued for
nine patients, and all three of the tracheostomy
tubes were removed. Of the five patients who con-
tinued to receive nourishment via the PEG, one was
lost to follow-up, one had a documented intracta-
ble hypertonic upper esophageal sphincter, and
three had persistently poor cough flows. No further
pulmonary complications occurred in these five
patients. None of the full oral feeders at the end of
the follow-up showed any nutritional or major
respiratory decompensation based on arterial blood
gas analyses or SpO2 and EtCO2 measurements.
DISCUSSION
The findings of this study show that the vol-
untary cough as measured using a peak flow meter,
can be considered a predictive factor for medium/
long-term pulmonary complications in patients
with dysphagia caused by upper airway surgery or
neurologic disorders and who aspirate. Conversely,
our results indicate that penetration, tracheal as-
piration, and the depth of penetration in the bron-
chial tree are not predictive of respiratory morbidity,
thus supporting the findings of Pikus et al.15
A recent study demonstrated that similar deg-
rees of oropharyngeal aspiration in different patients
may lead to early lung damage or be tolerated for a
long time without any apparent harm.16 Another
study has highlighted that the relationship between
documented oropharyngeal aspiration and respiratory
tract infections is still controversial by showing that
Am. J. Phys. Med. Rehabil. & Vol. 91, No. 6, June 2012
dysphagia alone is generally insufficient to cause as-
piration pneumonia.17 Despite the availability of ac-
curate diagnostic methods such as MBS, there is still a
lack of prognostic indicators of oral feeding safety.
One MBS study found that 27% of the patients with
tracheal aspiration were positive for pneumonia,
whereas only 35% of those with aspiration in the
bronchial tree were positive for pneumonia15; how-
ever, the authors did not explain why the remaining
patients did not develop pulmonary complications.
Most studies on the prevention of aspiration pneu-
monia have concentrated on the risk factors re-
lated to dysphagia, and none have investigated the
potential role of coughing. Coughing is typically
considered to be a merely reflexive mechanism
elicited by the mechanical or chemical stimulation
of the lower airways,18 but it can also be generated
voluntarily to clear the airways and can be used as a
precious defense mechanism.
To the best of our knowledge, this is the first
attempt to demonstrate the relevance of the vol-
untary cough measure as predictive of pulmonary
complications of dysphagia. The current literature
only describes the aerodynamic measure of volun-
tary cough as predictive of aspiration,19 whereas our
findings highlight a possible explanation for the
absence of respiratory complications despite tra-
cheobronchial aspiration in 62% of the examined
patients. Furthermore, we identified a CPF thresh-
old value of 242 liters/min as being capable of pre-
dicting the risk of pulmonary complications: CPF
levels less than 242 liters/min predicted pulmonary
morbidity in 65% of cases, and levels greater than
242 liters/min excluded pulmonary complications
in 90%. The patients who did not develop pulmo-
nary disorders but with their CPF under the
threshold were most likely protected by effective
pulmonary clearance despite the absence of cough
because this type of protective mechanism has
been shown in a scintigraphic swallowing study.20
Regarding the two patients in our series who de-
veloped pulmonary morbidity despite CPFs greater
than 242 liters/min, other risk factors may have
played a role.17
This study of limited sample size can be consid-
ered a first step toward explaining the difference in
pulmonary consequences in dysphagic patients with
persistent aspiration. Our primary findings support
the role of CPF in predicting pulmonary complica-
tions (identification of a threshold of 242 liters/min
and difference of 100 liters/min in CPF levels of
patients with and without pulmonary complications)
and are supported by adequate power of results
(980%), whereas a lesser value (a posteriori power:
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G60%) supported any relationship between the oc-
currence of a bronchogram and the development of
pulmonary complications. Further limitations derive
from the retrospective nature of the study. How-
ever, considering the lack of prospective studies in
this field, we believe that our results represent a
starting point for future research.
Our study also suggests a new rehabilitation
strategy to increase cough flows for dysphagic
patients as recently suggested in a case report.21
Some chronic aspirators can be allowed long-term
oral feeding (thus delaying or avoiding enteral
feeding) provided that their nutritional and respi-
ratory status is properly monitored.22,23
In conclusion, the objective and quantifiable
measure of cough flows is a promising tool for phy-
sicians and speech-language therapists involved in
the rehabilitation and follow-up of severe-dysphagia
patients, both for deciding feeding modalities and
for tailoring a rehabilitative strategy aimed at im-
proving oral feeding safety.
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