Dysphagia (2011) 26:295–303
DOI 10.1007/s00455-010-9311-3
ORIGINAL ARTICLE
Effects of Reduced Saliva Production on Swallowing in Patients
with Sjogren’s Syndrome
Nicole M. Rogus-Pulia • Jeri A. Logemann
Received: 13 March 2009 / Accepted: 18 September 2010 / Published online: 28 October 2010
Ó Springer Science+Business Media, LLC 2010
Abstract This study aimed to further characterize the
nature of swallowing dysfunction in patients with Sjogren’s
syndrome (SS). Subjects filled out a perception of swallow
function form. Measures of stimulated salivary flow rate
were also taken, and videofluoroscopic evaluation of
swallowing was completed. The amount of saliva produced
by patients with SS was significantly less than that pro-
duced by normal age-matched controls, and these patients
perceived their swallowing to be impaired. Few statistically
significant differences were found between the SS group
and normal age-matched controls on temporal measures of
swallowing, and 96% of swallows in the SS group were
judged to be functional. There was no correlation between
perception of swallowing and amount of saliva produced.
No strong correlations were found between temporal
measures of swallowing and salivary flow rate. Results
indicated that patients with SS tend to perceive their
swallowing to be worse than physiologic swallowing
measures indicate. The decreased saliva production in these
patients does not appear to be the cause of their perceived
swallowing difficulty but may affect their sensory judg-
ment of swallow function. Future studies will focus on how
quality of saliva affects swallowing in these patients.
N. M. Rogus-Pulia
J. A. Logemann
Department of Communication Sciences and Disorders,
Northwestern University, Evanston, IL 60208-3570, USA
N. M. Rogus-Pulia (&)
Department of Communication Sciences and Disorders,
Northwestern University, Swallowing Physiology Laboratory,
Frances Searle Building, 2240 Campus Drive, Evanston,
IL 60208-3570, USA
e-mail: nicoleroguspulia@gmail.com
Keywords Sjogren’s syndrome
Saliva
Temporal
measures
Swallowing physiology
Perception

Videofluoroscopy
Deglutition
Deglutition disorders
The critical role of saliva in protecting the oral cavity is
often unrealized until a shortage is experienced. Saliva
provides essential lubrication, pH neutralization, and pro-
tection from pathogens in the oral cavity. Hyposalivation
occurs when there is a reduction in the amount of saliva
produced by the salivary glands (a decreased salivary flow
rate). Xerostomia, the subjective perception of dry mouth,
usually accompanies hyposalivation [1, 2] but may occur
without a reduction in salivary flow rate as well [3, 4].
Swallowing often becomes difficult for those with hypo-
salivation and/or xerostomia [1].
Previous studies have examined the characteristics and
mechanism behind hyposalivation and xerostomia in
patients who have received treatment for head and neck
cancer. Loss of salivary gland function is a well-recognized
side effect of radiotherapy [1, 2, 5]. Along with hyposali-
vation and xerostomia, dysfunctional swallowing is a
common morbidity associated with radiation treatment for
head and neck cancer. For patients with salivary glands
included in the radiation field, various swallowing disor-
ders have been identified, including increased oral transit
time, reduced tongue base retraction, reduced laryngeal
elevation and closure, reduced duration of cricopharyngeal
opening, and increased pharyngeal transit time [6–23].
A study by Logemann et al. [24] examined the quantity
of saliva produced before onset of treatment with high-dose
chemoradiation and at 3 months post-treatment. This
quantity was examined in relation to patient perception of
swallowing and ability to propel food from the oral cavity
to the pharynx. Patients showed a significant decrease in
123
296 N. M. Rogus-Pulia, J. A. Logemann: Swallowing in Sjogren’s Syndrome Patients
saliva and an increased number of perceived swallowing
problems following treatment. In addition, patients with
swallowing complaints usually had lower saliva flow rates
than those without complaints of dysphagia at both eval-
uation times. However, the patients’ xerostomia did not
significantly affect the physiologic aspects of the bolus
transport, demonstrating that xerostomia may affect the
patients’ overall sensory perception more than actual
movement of the bolus. A follow-up study concluded that
changes in patients’ diet choices and comfort in eating (due
to reduced saliva production) persisted beyond 3 months
after treatment completion and that reduced saliva weight
does not correlate with the physiologic aspects of bolus
transport [25]. That study also indicated the need for fur-
ther examination into the effects of xerostomia resulting
from other etiologies [25].
One such etiology is the autoimmune disease called
Sjogren’s syndrome (SS). SS is a chronic inflammatory
disorder characterized by lymphocytic infiltration of the
exocrine glands, particularly the lacrimal and salivary
glands. It is characterized by what has been termed the ‘‘sicca
complex,’’ which refers to the decrease in tears and saliva
that results in keratoconjunctivitis sicca (KCS or dry eyes)
and xerostomia with or without hyposalivation [26–29].
In order to be diagnosed with SS, a patient must exhibit
at least two of the following: (1) definite KCS, (2) positive
lip biopsy that confirms the presence of lymphocytes as the
cause for dry mouth, and (3) associated extraglandular
connective tissue disease [26–33]. Xerostomia is often the
clinical presenting symptom and can lead to consideration
of this syndrome [31]. However, decreased salivary flow
rates are not always correlated with clinical complaints of
dry mouth and therefore are not diagnostic of SS [30, 34].
In addition to reduced flow rates, qualitative changes in
saliva have also been documented [31, 35–37].
In addition to hyposalivation and/or xerostomia, patients
with SS have also been found to suffer from dysfunctional
swallowing [11, 12, 38]. Previous studies examining
swallowing in patients with SS found that these patients
have both longer durations of hyoid movement and longer
pharyngeal transit times [11, 12, 38] as well as a perception
of impaired swallowing [11, 12]. Patients with SS even
have lower saliva production and perceive their swallowing
to be more impaired than patients treated for head and neck
cancer [12]. Although it has been suggested that some of
the difficulty with swallowing in these patients is due to
esophageal peristalsis [39–43], this does not explain why
those without esophageal issues also experience dysphagia.
Therefore, the nature of dysphagia and the relationship
between xerostomia and swallowing in this population
remains to be elucidated.
Therefore, the purpose of this study is to examine the
quantity of saliva produced by patients diagnosed with
123
primary SS and then to examine its relationship to their
subjective swallowing dysfunction and the physiologic
aspects of their swallowing. Furthermore, the information
obtained about this particular population will be compared
to data from normals. The two main research questions
addressed in this study are: (1) How do patients diagnosed
with SS compare to age- and gender-matched normals in
terms of salivary flow rate, swallow function, and percep-
tion of swallow ability? and (2) What is the relationship
between salivary flow rate and perception of swallow ability
as well as actual swallow function in patients with SS?
Methods and Procedures
There were two groups of subjects: (1) 20 patients diag-
nosed with primary or secondary SS and (2) 20 age- and
gender-matched control subjects (Table 1 for subject
characteristics). Subjects were recruited through the Rheu-
matology Department at Northwestern Memorial Hospital
(NMH), outside referrals, and local support group meetings.
Inclusion criteria included (1) diagnosis of primary or sec-
ondary SS by a medical doctor, (2) age 30-80 years, and (3)
xerostomia. Exclusion criteria included (1) a diagnosis of
primary or secondary SS but no complaints of dry mouth
and (2) other medical problems that are known to cause
xerostomia and/or dysphagia. The second group consisted
of 20 age- and gender-matched (±5 years) normal subjects
who were selected from archival databases. Data from these
subjects were used to compare physiologic swallowing
measures of patients with SS to normal values.
Each SS patient underwent three test procedures: (1) a
questionnaire consisting of 12 questions about the patient’s
perception of dry mouth and swallowing ability; (2) stim-
ulated whole saliva production evaluated by weighing a
4-in. 9 4-in. gauze pad before and after the patient chewed
the gauze for 2 min [33]; and (3) a videofluoroscopic study
of oropharyngeal swallowing during which the patient was
had to swallow two each of 1, 3, 5, and 10 ml of thin liquid,
3 ml of pudding consistency, and cookie [44]. Two hours
prior to the evaluation of stimulated whole saliva produc-
tion, subjects were instructed not to eat, drink, smoke, or
rinse their mouths until the test battery was completed. If
patients were taking salivary replacement medications (i.e.,
Salagen, Evoxac), they were instructed to discontinue use of
the medication 48 h in advance of the study. This evaluation
was performed in the afternoon when maximal saliva pro-
duction occurs [45]. The protocol was approved by the
Institutional Review Board of Northwestern University, and
all subjects signed informed consent statements.
Each videofluoroscopic study was analyzed to make 12
temporal measures of the oropharyngeal swallow, obser-
vations of residue in the oral cavity and pharynx, and
N. M. Rogus-Pulia, J. A. Logemann: Swallowing in Sjogren’s Syndrome Patients 297

Table 1 Subject characteristics

Subject Age Gender Sjogren’s Other medical problems
No. syndrome
diagnosis

1 55 F Primary None
2 69 F Secondary Fibromyalgia, duodenal ulcer, GERD, diverticulosis, gastritis
3 63 F Primary Hypertension
4 55 F Primary GERD, asthma
5 52 F Primary Clinical depression
6 39 F Secondary Scleroderma
7 41 F Primary None
8 43 F Secondary Primary biliary cirrhosis, goiter, GERD, ulcerative
colitis, osteoarthritis
9 62 F Secondary Rheumatoid arthritis, osteoarthritis, fibromyalgia,
scleroderma, GERD, osteoporosis
10 48 F Primary GERD
11 74 F Secondary Rheumatoid arthritis, gastroesophageal reflux
12 54 F Secondary Raynaud’s phenomenon, autoimmune thyroid disease,
migraine headaches
13 50 F Primary Hypertension, brain aneurysm s/p craniotomy for clipping
4 years prior
14 50 F Secondary CREST syndrome, Raynaud’s phenomenon
15 44 F Secondary Scleroderma, G.A.V.E., gastroesophageal reflux, epilepsy
16 43 F Secondary Fibromyalgia, inflammatory polyarthritis, hypertension, sleep
apnea, irritable bowel syndrome, gastroesophageal reflux,
clinical depression, migraine headaches
17 43 F Primary None
18 57 F Secondary Fibromyalgia, osteoporosis, osteoarthritis, fatty liver, aortic
insufficiency, hiatal hernia, ruptured discs (L3, L4, L5)
19 57 F Primary None
20 30 M Primary None

observations about the occurrence, amount, and timing of
penetration/aspiration. Clinical judgments on the presence
of certain oropharyngeal motility disorders were also noted
[46, 47] (Table 2). Each swallow was also designated as
functional or nonfunctional based on whether aspiration
occurred and the amount of residue.
The temporal measures can be divided into three cate-
gories: (1) five bolus transit measures, (2) six valve func-
tion measures, and (3) two tongue base measures (Table 3).
Two observations of residue were made: (1) approximate
percentage of the bolus remaining in the oral cavity after
the swallow and (2) the approximate percentage of the
bolus remaining in the pharynx after the swallow [48].
Observations of penetration and aspiration included (1)
whether penetration/aspiration occurred, (2) the approxi-
mate amount of bolus penetrated/aspirated, and (3) when
penetration/aspiration occurred.
Statistical Analysis
An independent sample t test was used to compare saliva
weight normative values [33] with saliva weight values for
the patients with SS. Fisher’s exact test was used to com-
pare approximate amount of residue, frequency of pene-
tration/aspiration, and frequency of oropharyngeal motility
disorders between normal control subjects and patients
with SS.
To determine the relationship between salivary flow rate
and perception of swallowing ability within the SS group,
data were arranged in two different ways. First, patients
with SS were divided into two groups based on their
answer to each question on the perception of function form.
For each question, the patients with SS were divided into
those who replied ‘‘yes’’ and those who replied ‘‘no’’ to
that particular question. Then, the flow rates for each of
these two groups for each question were compared using
the nonparametric Mann-Whitney U test. Second, the
patients with SS were divided into two groups based on the
number of ‘‘yes’’ answers they had given on the perception
of function form. If a patient gave six or fewer ‘‘yes’’
answers, that patient belonged to group 1. If a patient gave
more than six ‘‘yes’’ answers, that patient belonged to
group 2. The flow rates for each of these two groups were
compared using a t test.

123
298
Table 2 Clinically judged oropharyngeal motility disorders
Oropharyngeal motility disorders
Reduced lip closure
Reduced tongue strength
Reduced vertical movement of the oral
tongue
Reduced tongue control/shaping
Reduced manipulation and propulsion of
bolus in the mouth
Delayed pharyngeal swallow
Reduced tongue base retraction
Reduced laryngeal elevation
Unilateral or bilateral pharyngeal wall
weakness
Incomplete laryngeal vestibule closure
Reduced glottic closure/incomplete
laryngeal closure
Reduced cricopharyngeal opening
Table 3 Definitions of temporal measures
Bolus transit measures
Oral transit time
Pharyngeal delay time (PDT)
Pharyngeal response time (PRT)
Pharyngeal transit time
(PDT ? PRT)
Valve function measures
Velopharyngeal closure
Hyoid movement
Laryngeal elevation
Laryngeal vestibule closure
Cricopharyngeal opening
Base of tongue measures
Base of tongue to cervical
vertebra 2
Base of tongue to posterior
pharyngeal wall
Temporal measures were compared between normal
controls and the SS patients by performing mixed three-
way analyses of variance (2 9 2 9 6). The independent
123
N. M. Rogus-Pulia, J. A. Logemann: Swallowing in Sjogren’s Syndrome Patients
Definitions and signs/symptoms of disorders
Material falls from the mouth anteriorly.
Residue on the tongue or hard palate. Unable to strip bolus completely from tongue or palate.
Residue increases with increased viscosity.
Tongue does not elevate to make contact with the hard palate. Residue on the hard palate.
Bolus slips to the sides of tongue, over the top of tongue, or over tongue base. Inability to form a
cohesive bolus.
Multiple tongue pumps; difficulty in moving the bolus of the mouth to the back of the oral cavity.
Pharyngeal swallow does not trigger when the head of the bolus reaches the point where the tongue
base crosses the mandible.
Residue in the valleculae and possibly along the base of tongue. Inadequate contact between base of
tongue and posterior pharyngeal wall.
Residue in the pyriform sinuses or at the top of the airway; visually the larynx does not move
adequately (elevates less than 2 cm).
Residue on one or both sides of the pharyngeal wall. Anterior-posterior view used to distinguish
unilateral from bilateral.
Penetration or aspiration occurs during the swallow.
Aspiration during the swallow from the given bolus. Does not include aspiration after the swallow
from a previous bolus.
Residue in both pyriform sinuses, possibly in conjunction with reduced laryngeal elevation.
Definitions
Time from initial posterior movement of bolus in oral cavity until leading edge of bolus reached point
where lower rim of mandible crossed tongue base
Time when leading edge of bolus reached point where mandible crosses tongue base until laryngeal
elevation begins, indicating onset of pharyngeal motor response
Time between laryngeal elevation onset and last cricopharyngeal opening
Time when leading edge of bolus reached point where mandible crosses tongue base until point of last
cricopharyngeal opening
Time between first and last contact of superior-posterior aspect of soft palate with posterior pharyngeal
wall
Time between first forward movement of hyoid bone (associated with tongue base retraction) and return
to resting position
Time between first elevation of the larynx associated with the swallow and return to resting position
Time between first point of closure within the laryngeal vestibule and the point immediately preceding
airspace reappearance within the vestibule
Time between first separation of tracheal and esophageal walls (at level 1 cm below true vocal folds) and
point at which bolus clears this level.
Duration of tongue base contact with posterior pharyngeal wall at level of inferior portion of cervical
vertebra 2
Time between onset of tongue base movement and point where tongue base contacts posterior pharyngeal
wall
variables included one between-subjects variable, group,
with two levels (SS and normal), a within-subjects vari-
able, trial, with two levels (first and second), and another
N. M. Rogus-Pulia, J. A. Logemann: Swallowing in Sjogren’s Syndrome Patients 299

within-subjects variable, bolus type, with six levels (1-, 3-,
5-, and 10-cc thin liquid boluses, a 3-cc paste bolus, and a
cookie bolus).
Pearson product-moment correlation coefficients were
calculated to determine the relationship between saliva
weight and temporal measures. These correlation coeffi-
cients were calculated separately for each of the six bolus
types and also for temporal measures averaged across bolus
type. Temporal measures were all averaged across trial.
Before conducting this analysis, correlations between each
of the temporal measures were calculated to determine
whether two measures (or more) were essentially measur-
ing the same aspect of the swallow (a significant correla-
tion coefficient). If this was the case, only one of the related
measures was correlated with flow rate. The temporal
measures that were eliminated due to multicolinearity
varied depending upon the bolus type.
Results
Difference in Saliva Weight Between Groups
The 20 patients with SS exhibited significantly lower saliva
weights in grams than saliva weight normative values taken
from Kohler and Winter [33] (Table 4).
Table 4 Saliva weight in normals versus SS patients
Normal controlsa SS patients P value
(N = 25) (N = 20)
Mean salivary flow rate 4.24 (0.21)b 2.01 (0.43) 0.000c
a
Data for normals from Kohler and Winter (1985)
b
Levene’s test for equality of variances was significant (P = 0.031),
so equal variances were not assumed
c
P \ 0.05
Frequency of Clinically Judged Oropharyngeal Motility
Disorders
A significant increase in the frequency of the following
oropharyngeal motility disorders in the SS group was
found: delayed pharyngeal swallow for cookie bolus, trial 1
(P = 0.047); reduced tongue base retraction for paste
bolus, trial 2 (P = 0.032), and cookie bolus, trial 1
(P = 0.0083) (Table 2 for definitions of disorders). It is
important to note, however, that 97% of swallows were
judged to be functional (without aspiration or significant
residue) in the SS group.
Main Effects for Temporal Measures
Selected results for the mixed three-way analyses of vari-
ance for each temporal measure are displayed in Table 5.
For the following temporal measures, significant main
effects for the independent variable group were found: base
of tongue to posterior pharyngeal wall, base of tongue to
cervical vertebra 2, and cricopharyngeal opening (Fig. 1).
Interaction Effects for Temporal Measures
A significant interaction between bolus type and group was
found for the base of tongue to posterior pharyngeal wall
measure. There are two possibilities for what this interac-
tion might have indicated: (1) group differences on this
measure were present for only certain bolus types, or (2)
there were significant differences between bolus types
within one group but not within the other group. To further
clarify this interaction, post-hoc analysis was performed
using paired-sample t tests with a Bonferroni correction
first to compare the two groups (patients with controls) by
bolus type and second to compare the different bolus types
within each separate group. Significant group differences
were found for all bolus types, but significant differences

Table 5 Selected ANOVA

Temporal measures Main effect for group Bolus type 9 group
results for temporal measures
Oral transit time F = 0.102; P = 0.752 F = 1.884; P = 0.17
Base of tongue to posterior pharyngeal wall F = 141.2; P = 0.000* F = 4.44; P = 0.046*
Base of tongue to cervical vertebra 2 F = 18.46; P = 0.000* F = 1.148; P = 0.323
Velopharyngeal closure F = 0.013; P = 0.911 F = 0.844; P = 0.469
Hyoid movement F = 0.694; P = 0.694 F = 1.346; P = 0.264
Laryngeal elevation F = 0.154; P = 0.389 F = 1.154; P = 0.331
Laryngeal vestibule closure F = 0.04; P = 0.843 F = 1.526; P = 0.21
Cricopharyngeal opening F = 5.149; P = 0.029* F = 1.253; P = 0.292
Laryngeal closure to cricopharyngeal opening F = 1.843; P = 0.183 F = 3.124; P = 0.046*
Pharyngeal response time (PRT) F = 0.502; P = 0.483 F = 1.3; P = 0.276
Pharyngeal delay time (PDT) F = 2.438; P = 0.127 F = 1.24; P = 0.282
Pharyngeal transit time (PRT ? PDT) F = 2.648; P = 0.112 F = 1.693; P = 0.201
* P \ 0.05

123
300 N. M. Rogus-Pulia, J. A. Logemann: Swallowing in Sjogren’s Syndrome Patients

0.6 Comparison of Frequency of Penetration and Aspiration

Time duration (in seconds)

0.5 Between Groups

There were significantly more occurrences of penetra-
0.4
tion in the SS group (8 of 240 boluses) than in the control
0.3 group (0 of 240 boluses; P \ 0.01). There was not a sig-
0.2 nificant difference in occurrence of aspiration between the
0.1
groups (1 occurrence in SS group, 0 in control group).

6E-16
-0.1
Controls Sjogren’s Controls
BOT to PPW
Temporal Measures
Fig. 1 Significant main effects for group variable on three temporal
measures: BOT to PPW (base of tongue to posterior pharyngeal wall),
BOT to C2 (base of tongue to cervical vertebrae 2), and CPO
(cricopharyngeal opening)
across bolus type existed only in the SS group. In the SS
group, it took the base of tongue longer to come into
contact with the posterior pharyngeal wall when the bolu-
ses were smaller (1-, 3-, and 5-ml vs. 10-ml thin liquid
bolus) and thinner (3-ml thin liquid vs. cookie boluses).
In addition, there was a significant interaction present
between bolus type and group for the laryngeal closure to
cricopharyngeal opening measure. Post-hoc analysis
revealed significant differences across bolus types within
the SS group but not within the control group. The lar-
yngeal closure to cricopharyngeal opening measure was
longer for thicker-consistency boluses than for thinner
consistency boluses.
Relationship Between Temporal Measures and Flow
Rate Within SS Group
Sjogren’s Controls Sjogren’s
BOT to C2 CPO
Results showed that two of the temporal measures were
significantly correlated with salivary flow rate (Fig. 3). A
significant, positive correlation was observed between oral
transit time and flow rate for 5-ml thin liquid. A significant,
negative correlation was found between pharyngeal
response time and flow rate for paste. Even though the
correlations between these measures and flow rate were
statistically significant, they were weak correlations and
only occurred for one bolus type.
Relationship Between Residue and Flow Rate Within
SS Group
Percentages of oral and pharyngeal residue were not sig-
nificantly correlated with flow rate on any of the boluses.
Relationship Between Perception and Flow Rate Within
SS Group

Comparison of Residue Between Groups Results for the comparison in flow rates between those who
answered ‘‘yes’’ and those who answered ‘‘no’’ to each
Main effects were found for group on approximate per- question on the perception of function form can be found in
centage of oral (P \ 0.05) and pharyngeal (P \ 0.01) Table 6. None of the tests were significant, leading to the
residue (Fig. 2). A significantly larger amount of oral and conclusion that flow rates did not differ significantly based
pharyngeal residue was found in the SS group. on the answer to each question.

6 OTT on 5 mL thin liquid

PRT on Paste
8
Flow rate (in grams)

5 7
6
r=0.54 r=-0.47
4 5
Percentage

4
3 3
2
2
1
0
1
Controls Sjogren’s Controls Sjogren’s
0 0.2 0.4 0.6 0.8 1 1.2
BOT to C3 CPO
Time (in seconds)
0
Controls Sjogren’s Controls Sjogren’s
Oral Residue Pharyngeal Residue Fig. 3 Significant correlations between flow rate and two of the
temporal measures, OTT (oral transit time) on a 5-ml thin-liquid
Fig. 2 Significant main effects for group for approximate percent- bolus and PRT (pharyngeal response time) on a paste bolus.
ages of oral (P \ 0.05) and pharyngeal residue (P \ 0.01) Triangles, oral transit time; Squares, pharyngeal response time

123
N. M. Rogus-Pulia, J. A. Logemann: Swallowing in Sjogren’s Syndrome Patients 301

Table 6 Comparison of mean

Perceived problem Number who Number who Mean saliva Mean saliva P
saliva weight (g) between those
responded responded weight for weight for
who answered ‘‘yes’’ vs. those
‘‘yes’’ ‘‘no’’ ‘‘yes’’ group ‘‘no’’group
who answered ‘‘no’’ to each
question on the perception of Swallowing problems 19 1 1.98 2.52 0.544
function form
Dry mouth 20 0 2.01 All yes N/A
Food sticks in mouth 18 2 1.67 5.03 0.099
Food sticks in throat 18 2 1.97 2.30 0.544
Food will not go down 17 3 1.88 2.73 0.795
Need water assist 20 0 2.01 All yes N/A
Choking 16 4 2.09 1.68 0.931
Coughing 14 6 1.57 3.02 0.099
Food liquid comes up 10 10 2.45 1.56 0.795
Heartburn 16 4 2.42 0.37 0.340
Night cough/gag 9 11 2.17 1.87 0.099
Change in taste 14 6 1.85 2.37 0.099

Discussion thicker boluses. The clinical observation of reduced base of

The amount of saliva produced in the patients with SS was
significantly lower than in the normal subjects in this study.
In addition, generally patients with SS tend to perceive
their swallowing to be impaired. Despite this perception,
only 3 of the 12 temporal measures in the SS group differed
significantly from normal. In the SS patients, it took longer
for the base of tongue to contact the posterior pharyngeal
wall, and it did not maintain contact as long. This effect
became more pronounced with smaller and thinner bolus
types in the SS group only. These differences in the base of
tongue measures may have affected the amount and rate of
pressure generation in the SS group. In addition, the SS
group demonstrated longer cricopharyngeal opening, and
their laryngeal closure to cricopharyngeal opening duration
measure increased with thicker boluses. It may be
hypothesized that changes in these measures with thicker
boluses demonstrate a successful compensatory response to
decreased lubrication and resultant slowed movement of
the bolus, as pharyngeal transit times were not prolonged in
this group. Interestingly, even though a few of the temporal
measures differed significantly between groups, 97% of the
swallows in the patients with SS were clinically judged to
be functional.
The patients with SS did have significantly more oral
and pharyngeal residue following their swallow. However,
the average amounts of residue were below 5%, which is
clinically insignificant. There were more occurrences of
penetration in the SS group, but the incidence was extre-
mely low at 3% when contrasted with normative data on
frequency of penetration, which ranged from 7.4 to 16.8%
depending on age [49].
In regards to clinical judgments of motility disorders, SS
subjects were more likely to be diagnosed with a delayed
pharyngeal swallow and reduced tongue base retraction on
tongue retraction is consistent with observed differences in
temporal measures seen in the SS group.
After determining how the physiologic measures of
swallowing in SS patients compared to controls, the rela-
tionship between salivary flow rate and temporal measures
was addressed. A significant relationship between flow rate
and temporal measures was observed in only two of a
potential 72 instances where a relationship could have
existed: oral transit time for 5-ml thin liquid and pharyn-
geal response time on paste. Combining this low number of
instances and the weak correlation coefficients (0.54-0.47,
respectively), one may conclude that the amount of saliva
produced is not a significant contributing factor in any of
the abnormal aspects of the swallow in SS patients. The
authors’ hypothesis that the relationship between temporal
measures and flow rate would have become more pro-
nounced on thicker boluses was not supported by these
findings.
Therefore, if all swallows were judged to be functional
and few of the temporal measures differed from normal,
the question remains as to why these patients overwhelm-
ingly report very impaired swallowing. Although it was
hypothesized that flow rate may be underlying these per-
ceptions of impairment, results did not reveal a relation-
ship. Therefore, the basis for perceived impairment in this
group remains unclear and an area for future research.
There were several limitations to this study that could
have potentially affected results. First, data for normal
controls was taken retrospectively. Second, the patients
with SS differed in time since diagnosis, diagnostic criteria
(clinical vs. biopsy), and severity of symptoms. Third,
recruitment of males with SS as well as those with primary
(vs. secondary) SS was difficult. The majority of our
patients were females with secondary SS, thereby limiting
the ability to generalize these results.

123
302 N. M. Rogus-Pulia, J. A. Logemann: Swallowing in Sjogren’s Syndrome Patients
Future research needs to focus on determining why these
patients perceive their swallowing to be more impaired
than physiologic measures indicate. Since salivary flow
rate did not factor into differences between groups on
temporal measures or patient perception of function,
altered salivary composition is one possible explanation.
Salivary mucoglycoproteins, which have been identified as
important for lubrication and hydration of oral mucosa and
communication of sensory signals in the oropharynx, are of
particular interest [50]. SS patients suffer from autoim-
mune salivary gland destruction and subsequent decreased
levels of these proteins [51]. Chronic low levels of these
critical proteins may alter sensation and result in the per-
ception of impaired swallowing. Another possible expla-
nation for the discrepancy between perception and
physiologic swallow function could be potential effects of
hormonal changes related to menopause on saliva and the
sensory system, especially since 90% of SS patients are
perimenopausal females [52]. Further investigation should
aim to explore other factors such as salivary composition
and hormonal changes, which may mediate the relationship
between function and perception of swallowing in the SS
population.
References
1. Levine RS. Saliva: 3. Xerostomia—aetiology and management.
Dental Update. 1989;16:197–201.
2. Navazesh M, Ship I. Xerostomia: diagnosis and treatment. Am
J Otolaryngol. 1983;4(4):283–92.
3. Wolowski A, Runte C, Helms S. Oral dryness: subjective per-
ceptions and objective causes. J Am Geriatr Soc. 2003;51(11):
1678–9.
4. Won S, Kho H, Kim Y, Chung S, Lee S. Analysis of residual
saliva and minor salivary gland secretions. Arch Oral Biol.
2001;46(7):619–24.
5. Schubert MM, Izutsu KK. Iatrogenic causes of salivary gland
dysfunction. J Dent Res. 1987;66:680–8.
6. Mossman KL, Scheer AC. Complications of radiotherapy of head
and neck cancer. Ear Nose Throat J. 1977;56(3):145–9.
7. Lazarus C. Effects of radiation therapy and voluntary maneuvers
on swallow functioning in head and neck cancer patients. Clin
Commun Disord. 1993;3(4):11–20.
8. Pauloski B, Logemann JA, Rademaker AW, McConnel FM,
Heiser MA, Cardinale S, Shedd D, Lewin J, Baker SR, Graner D,
Cook B, Milianti F, Collins S, Baker T. Speech and swallowing
function after anterior tongue and floor of mouth resection with
distal flap reconstruction. J Speech Lang Hear Res. 1993;
36(2):267–76.
9. Lazarus C, Logemann JA, Kahrilas PJ, Mittal BB. Swallow
recovery in an oral cancer patient following surgery, radiother-
apy, and hyperthermia. Head Neck. 1994;16:259–65.
10. Pauloski B, Logemann JA, Rademaker AW, McConnel F, Stein
D, Beery Q, Johnson J, Heiser MA, Cardinale S, Shedd D, Graner
D, Cook B, Milianti F, Collins S, Baker T. Speech and swal-
lowing function after oral and oropharyngeal resections: one-year
follow-up. Head Neck. 1994;16:313–22.
123
11. Rhodus N, Colby S, Moller K, Bereuter J. Quantitative assess-
ment of dysphagia in patients with primary and secondary Sjo-
gren’s syndrome. Oral Surg Oral Med Oral Pathol Oral Radiol
Endodontol. 1995;79:305–10.
12. Rhodus N, Moller K. Dysphagia in patients with three different
etiologies of salivary gland dysfunction. Ear Nose Throat J
1995;74 (1):39–42, 45–48.
13. Lazarus CL, Logemann JA, Pauloski BR, Colangelo LA, Kahrilas
PJ, Mittal BB, Pierce M. Swallowing disorders in head and neck
cancer patients treated with radiotherapy and adjuvant chemo-
therapy. Laryngoscope. 1996;106:1157–66.
14. Hamlet S, Faull J, Klein B, Aref A, Fontanesi J, Stachler R,
Shamsa F, Jones L, Simpson M. Mastication and swallowing in
patients with postirradiation xerostomia. Int J Radiat Oncol Biol
Phys. 1997;37(4):789–96.
15. Logemann J, Pauloski BR, Rademaker AW, Colangelo LA.
Super-supraglottic swallow in irradiated head and neck cancer
patients. Head Neck. 1997;19:535–40.
16. Newman LA, Vieira F, Schwiezer V, Samant S, Murry T,
Woodson G, Kumar P, Robbins KT. Eating and weight changes
following chemoradiation therapy for advanced head and neck
cancer. Arch Otolaryngol Head Neck Surg. 1998;124(5):589–92.
17. Pauloski BR, Rademaker AW, Logemann JA, Colangelo LA.
Speech and swallowing in irradiated and nonirradiated postsur-
gical oral cancer patients. Otolaryngol Head Neck Surg.
1998;118(5):616–24.
18. Kotz T, Abraham S, Beitler JJ, Wadler S, Smith RV. Pharyngeal
transport dysfunction consequent to an organ-sparing protocol.
Otolaryngol Head Neck Surg. 1999;125(4):410–3.
19. Kendall KA, Leonard RJ, McKenzie SW, Jones CU. Timing of
swallowing events after single-modality treatment of head and
neck carcinomas with radiotherapy. Ann Otol Rhinol Laryngol.
2000;109:767–75.
20. Pauloski B, Logemann JA. Impact of tongue base and posterior
pharyngeal wall biomechanics on pharyngeal clearance in irra-
diated postsurgical oral and oropharyngeal cancer patients. Head
Neck. 2000;22:120–31.
21. Newman L, Robbins KT, Logemann JA, Rademaker AW, Laz-
arus CL, Hamner A, Tusant S, Fang Huang C. Swallowing and
speech ability after treatment for head and neck cancer with
targeted intraarterial versus intravenous chemoradiation. Head
Neck. 2002;24:68–77.
22. Mittal B, Pauloski BR, Haraf DJ, Pelzer HJ, Argiris A, Vokes EE,
Rademaker A, Logemann JA. Swallowing dysfunction—pre-
ventative and rehabilitation strategies in patients with head-and-
neck cancers treated with surgery, radiotherapy, and chemother-
apy: a critical review. Int J Radiat Oncol Biol Phys. 2003;57(5):
1219–30.
23. Logemann JA, Rademaker AW, Pauloski BR, Lazarus CL, Mittal
BB, Brockstein B, MacCracken E, Haraf DJ, Vokes EE, Newman
LA, Dachao L. Site of disease and treatment protocol as correlates
of swallowing function in patients with head and neck cancer
treated with chemoradiation. Head Neck. 2005;28(1):64–73.
24. Logemann JA, Smith CH, Pauloski BR, Rademaker AW, Lazarus
CL, Colangelo LA, Mittal B, MacCracken E, Gaziano J, Stac-
howiak L, Newman LA. Effects of xerostomia on perception and
performance of swallow function. Head Neck. 2001;23:317–21.
25. Logemann JA, Pauloski BR, Rademaker AW, Lazarus CL, Mittal
B, Gaziano J, Stachowiak L, MacCracken E, Newman LA.
Xerostomia: 12-month changes in saliva production and its
relationship to perception and performance of swallow function,
oral intake, and diet after chemoradiation. Head Neck.
2003;25:432–7.
26. Talal N. Salivary and oral conditions. In: Carsons S, Harris EK,
editors. The New Sjogren’s Syndrome Handbook. New York:
Oxford University; 1998. p. 3–10.
N. M. Rogus-Pulia, J. A. Logemann: Swallowing in Sjogren’s Syndrome Patients
27. Fox RI. Epidemiology, pathogenesis, animal models, and treatment
of Sjogren’s syndrome. Curr Opin Rheumatol. 1994;6:501–8.
28. Fox RI. Salivary and oral conditions. In: Carsons S, Harris EK,
editors. The New Sjogren’s Syndrome Handbook. New York:
Oxford University; 1998. p. 11–23.
29. Bloch KJ, Buchanan WW, Wohl MJ, Bunim JJ. Sjogren’s syn-
drome: a clinical, pathological, and serological study of sixty-two
cases. Medicine. 1965;44(3):187–231.
30. Vitali C, Bombardieri S, Moutsopoulos HM, Balestrieri G,
Bencivelli W, Bernstein RM, Bjerrum KB, Braga S, Coll J,
DeVita S, Drosos AA, Ehrenfeld M, Hatron PY, Hay EM, Isen-
berg D, Janin A, Kalden J, Kater L, Konttinen YT, Maddison P,
Maini RN, Manthorpe R, Meyer O, Ostuni P, Pennec Y, Prause
JU, Richards A, Sauvezie B, Schiodt M, Sciuto M, Scully C,
Shoenfeld Y, Skopouli FN, Smolen J, Snaith M, Tishler M,
Todesco S, Valesini G, Venables P, Wattiaux M, Youinou P.
Preliminary criteria for the classification of Sjogren’s syndrome.
Arthritis Rheum. 1993;36(3):340–7.
31. Daniels TE, Silverman S, Michalski JP, Greenspan JS, Sylvester
RA, Talal N. The oral component of Sjogren’s syndrome. Oral
Med. 1975;39(6):875–85.
32. Robinson DA, Meyer CF. Primary Sjogren’s syndrome associated
with recurrent sinopulmonary infections and bronchiectasis.
J Allergy Clin Immunol. 1994;94:263–4.
33. Kohler PF, Winter ME. A quantitative test for xerostomia. The
Saxon test, an oral equivalent of the Schirmer test. Arthritis
Rheum. 1985;28:1128.
34. Daniels TE. Labial salivary gland biopsy in Sjogren’s syndrome.
Arthritis Rheum. 1984;27(2):147–56.
35. Chisholm DM, Beeley JA, Mason DK. Salivary proteins in
Sjogren’s syndrome: separation by isoelectric focusing in acryl-
amide gels. Oral Surg Oral Med Oral Pathol Oral Radiol Edod-
ontol. 1973;35(5):620–30.
36. Mandel ID, Baurmash H. Biochemical profile in salivary gland
disease. J Dent Res 1973;52: abstr No. 672.
37. Kalk WW, Vissink A, Spijkervet FK, Bootsma H, Kallenberg
CG, Nieuw Amerongen AV. Sialometry and sialochemistry:
diagnostic tools for Sjogren’s syndrome. Ann Rheum Dis.
2001;60:1110–6.
38. Caruso AJ, Sonies BC, Atkinson JC, Fox PC. Objective measures
of swallowing in patients with primary Sjogren’s syndrome.
Dysphagia. 1989;4:101–5.
39. Anselmino M, Zaninotto G, Constantini M, Ostuni P, Ianniello A,
Boccu C, Doria A, Todesco S, Ancona E. Esophageal motor
function in primary Sjogren’s syndrome: correlation with dys-
phagia and xerostomia. Dig Dis Sci. 1997;42(1):113–8.
40. Volter F, Fain O, Mathieu E, Thomas M. Esophageal function
and Sjogren’s syndrome. Dig Dis Sci. 2004;49:248–53.
303
41. Palma R, Freire A, Freitas J, Morbey A, Costa T, Saraiva F,
Queiros F, Carvalhinhos A. Esophageal motility disorders in
patients with Sjogren’s syndrome. Dig Dis Sci. 1994;39(4):
758–61.
42. Kjellen G, Fransson SG, Lindstrom F, Sokjer H, Tibbling L.
Esophageal function, radiography, and dysphagia in Sjogren’s
syndrome. Dig Dis Sci. 1986;31(3):225–9.
43. Grande L, Lacima G, Ros E, Font J, Pera C. Esophageal motor
function in primary Sjogren’s syndrome. Am J Gastroenterol.
1993;88(3):378–81.
44. Logemann J. Evaluation and treatment of swallowing disorders.
2nd ed. San Diego: College Hill; 1998.
45. Dawes C. Physiological factors affecting salivary flow rate, oral
sugar clearance, and the sensation of dry mouth in man. J Dent
Res. 1987;66:648–53.
46. Logemann JA. Manual for videofluoroscopic study of swallow-
ing. 2nd ed. Austin, TX: Pro-Ed; 1993.
47. Pauloski BR, Rademaker AW, Logemann JA, Newman L,
MacCracken E, Gaziano J, Stachowiak L. Relationship between
swallow motility disorders on videofluorography and oral intake
in patients treated for head and neck cancer with radiotherapy
with or without chemotherapy. Head Neck. 2006;28(12):
1069–76.
48. Logemann JA, Williams RB, Rademaker AW, Pauloski BR,
Lazarus CL, Cook I. The relationship between observations and
measures of oral and pharyngeal residue from videofluorography
and scintigraphy. Dysphagia. 2005;20:226–31.
49. Daggett A, Logemann JA, Rademaker A, Pauloski B. Laryngeal
penetration during deglutition in normal subjects of various ages.
Dysphagia. 2006;21(4):270–4.
50. Engelen L, van den Keybus PA, de Wijk RA, Veerman EC,
Amerongen AV, Bosman F, Prinz JF, van der Bilt A. The effect
of saliva composition on texture perception of semi-solids. Arch
Oral Biol. 2007;52(6):518–25.
51. Almstahl A, Wikstrom M, Groenink J. Lactoferrin, amylase, and
mucin MUC5B and their relation to the oral microflora in
hyposalivation of different origins. Oral Microbiol Immunol.
2001;16:345–52.
52. Pillemer SR, Matteson EL, Jacobsson LT, Martens PB, Melton
LJ. Incidence of physician-diagnosed primary Sjogren syndrome
in residents of Olmsted County, Minnesota. Mayo Clin Proc.
2001;76(6):593–9.
Nicole M. Rogus-Pulia MA
Jeri A. Logemann PhD
123