Dysphagia

https://doi.org/10.1007/s00455-019-09992-x

ORIGINAL ARTICLE

Association Between Pharyngeal Pooling and Aspiration Using

Fiberoptic Endoscopic Evaluation of Swallowing in Head and Neck
Cancer Patients with Dysphagia
Sorina R. Simon1 · Michelle Florie1 · Walmari Pilz1,2 · Bjorn Winkens3,4 · Naomi Winter1 · Bernd Kremer1,2 ·
Laura W. J. Baijens1,2

Received: 21 June 2018 / Accepted: 23 February 2019

© The Author(s) 2019

Abstract
Postswallow pharyngeal pooling may be a risk factor for tracheal aspiration. However, limited literature shows the potential
association between pharyngeal pooling and aspiration in head and neck cancer (HNC) patients. This study investigates the
relationship between postswallow pharyngeal pooling and aspiration in HNC patients with oropharyngeal dysphagia. Fur-
thermore, the effects of tumor stage, tumor location, and cancer treatment on aspiration were examined. Ninety dysphagic
HNC patients underwent a standardized fiberoptic endoscopic evaluation of swallowing (FEES) using thin and thick liquid
boluses. For each swallow, three visuoperceptual ordinal variables were scored: postswallow vallecular pooling, postswal-
low pyriform sinus pooling, and aspiration. Logistic regression analyses with correction for the location of pooling, tumor
stage, tumor location, and cancer treatment were performed to explore the association between pooling and aspiration. No
significant association was found between postswallow vallecular pooling and aspiration for thin liquid. However, severe
versus mild-to-moderate postswallow vallecular pooling of thick liquid was significantly associated to aspiration. Similar
results were seen after correction for the presence of pyriform sinus pooling, tumor stage, tumor location, or type of cancer
treatment. This study showed a significant association between severe postswallow pyriform sinus pooling of thick liquid and
aspiration, independent of the presence of vallecular pooling, tumor stage, tumor location, or cancer treatment. Concluding,
location (valleculae versus pyriform sinuses), liquid bolus consistency (thin versus thick liquid), and amount of postswallow
pharyngeal pooling (no pooling, mild/moderate pooling, severe pooling) have an influence on the probability of aspiration
in dysphagic HNC patients, and they should be carefully considered during FEES, even in the absence of aspiration during
the examination.

Keywords Deglutition · Deglutition disorders · Pharyngeal pooling · Aspiration · Head and neck cancer · Fiberoptic
endoscopic evaluation of swallowing

Introduction
Electronic supplementary material The online version of this
article (https​://doi.org/10.1007/s0045​5-019-09992​-x) contains
supplementary material, which is available to authorized users. Oropharyngeal dysphagia (OD) is common among patients
with head and neck cancer (HNC) with a prevalence of
Sorina R. Simon and Michelle Florie have contributed equally to 60–75% [1]. In this population, OD can be a result of the
this work.

3
* Sorina R. Simon Department of Methodology and Statistics, Maastricht
[email protected] University, Maastricht, The Netherlands
4
1 Care and Public Health Research Institute – CAPHRI,
Department of Otorhinolaryngology, Head and Neck
Maastricht University Medical Center, Maastricht,
Surgery, Maastricht University Medical Center, P.O.
The Netherlands
Box 5800, 6202 AZ Maastricht, The Netherlands
2
School for Oncology and Developmental Biology –
GROW, Maastricht University Medical Center, Maastricht,
The Netherlands

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 S. R. Simon et al.: Association Between Pharyngeal Pooling and Aspiration

disease itself or its treatment. Treatment-induced alterations analysis, a different swallowing assessment tool (VFSS)
that contribute to OD include xerostomia, lymphedema, without standardized bolus consistencies was used, and not
fibrosis, and damage to neuromuscular structures. Further- all patients suffered from OD. To our knowledge, no studies
more, chemoradiotherapy and the presence of hypopharyn- have explored the potential association between postswallow
geal carcinoma are associated with an increased risk for late pharyngeal pooling and aspiration in a more general HNC
OD [2]. Common symptoms of swallowing impairment in population using FEES. The purpose of this study was to
HNC patients while eating include complaints of food ‘stick- determine the association between postswallow pharyngeal
ing’ in the throat, nasal regurgitation, coughing, or choking pooling and aspiration in HNC patients with OD, using a
[3]. OD following oncologic treatment can lead to dietary standardized FEES protocol. The influences of tumor stage,
restrictions, dehydration, malnutrition, aspiration pneumo- tumor location, and cancer treatment on the association were
nia, and death [4–6]. Therefore, an evaluation of swallow- also investigated.
ing complaints in patients with OD of oncological origin is
highly recommended. To evaluate the pharyngeal phase of
swallowing, fiberoptic endoscopic evaluation of swallowing Methods
(FEES) is deemed a reliable, safe, and well-tolerated tool.
It provides a direct, two-dimensional view of the pharyn- Participants
geal surface anatomy with a clear visualization of the bolus
path [7]. Using FEES, the safety (aspiration) and efficacy HNC patients with complaints of OD who underwent a
(pooling) of swallowing can be evaluated [8–10]. Several FEES examination at the Maastricht University Medi-
studies used FEES to evaluate the swallowing function, but cal Center outpatient clinic between 2009 and 2016 were
few used this method to assess OD in the HNC population enrolled in the study. The study sample comprised patients
[11, 12]. The visualization of aspiration during swallowing drawn from a routine outpatient clinic and they were invited
assessment in HNC patients has received much attention due to participate if the inclusion/exclusion criteria were met.
to its potentially severe consequences, including aspiration Patients were included if HNC treatment (surgery, radio-
pneumonia, sepsis, and death. Therefore, aspiration of food therapy, chemoradiotherapy, or combinations—multimodal-
or liquids in patients with HNC is a major concern, with a ity treatment) had been completed at least 6 months before
reported incidence rate ranging from 36 to 94% [13]. Factors the data collection and FEES examination, and if the dis-
associated with aspiration are advanced age and tumor stage, ease was in a stable period (total remission, the absence of
previous history of head and neck surgery, and/or chemo- radiation mucositis, or severe odynophagia). None of the
therapy [13]. As postswallow pharyngeal pooling is assumed patients was receiving palliative care. The following exclu-
to pose a risk for tracheal aspiration on the subsequent swal- sion criteria were applied: HNC and a concurrent neurologic
low, the detection of pooling during swallowing assessment disease; a Mini Mental State Examination score below 23;
is also becoming increasingly important [14]. Postswallow older than 85 years; having undergone a total laryngectomy;
pharyngeal pooling is defined as any portion of the bolus having a recurrent HNC or a second primary tumor, and
remaining in the valleculae and/or pyriform sinuses after the osteoradionecrosis of the maxilla or mandible. Cancer stag-
swallow, and it is considered to be a sign of impairment of ing according to the tumor, nodes, and metastasis (TNM)
deglutition [15, 16]. Reduced base-of-tongue retraction with classification system was performed [17]. Informed consent
loss of contact to the posterior pharyngeal wall and incom- was obtained from all patients in the outpatient clinic. The
plete cricopharyngeal relaxation can result in pharyngeal study protocol is classified as non-WMO dutiful according
pooling. This in turn may lead to postswallow aspiration, as to the Dutch Medical Research Human Subjects Act (http://
observed during a videofluoroscopic swallow study (VFSS) www.ccmo.nl/en/non-wmo-resea​rch).
in HNC patients [15]. Yet there is only limited literature
regarding the possible association between postswallow Swallowing Protocol
pharyngeal pooling and aspiration in patients with HNC.
Previous studies demonstrated that postswallow pharyngeal A standardized examination protocol used in the dysphagia
pooling is associated with aspiration during FEES exami- outpatient clinic for regular health care was applied. The
nation in patients with nasopharyngeal carcinoma treated protocol included a clinical ear, nose, and throat examination
with definitive radiotherapy [11, 12]. However, these studies comprising integrity of cranial nerves performed by a laryn-
only included patients with nasopharyngeal carcinoma, and gologist, the Functional Oral Intake Scale (FOIS) [7], and a
therefore their findings cannot be generalized to the overall standardized FEES examination [18]. The FOIS is used as
HNC population, although, Jung et al. found an associa- a standardized measurement in daily clinical practice in the
tion between the presence of vallecular pooling and aspira- outpatient clinic for OD (heterogeneous etiologies of OD
tion in patients with HNC [13]. During their retrospective are present, not only HNC). It is used as part of a structured

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S. R. Simon et al.: Association Between Pharyngeal Pooling and Aspiration

interview (descriptive variable) to assess the level of oral (or the valleculae up to complete filling). Postswallow pyriform
nonoral) intake. FOIS scores range from one (‘nothing by sinus pooling was scored as no pooling (‘0’), mild-to-mod-
mouth’) to seven (‘total oral diet with no restrictions’) [7]. erate pooling (‘1’: filling of less than 50% of the pyriform
The FOIS provides an overall picture of which patients use sinuses), or severe pooling (‘2’: filling of more than 50% of
a modified texture diet or tube feeding, and which patients the pyriform sinuses up to complete filling). Severe pooling
have a total oral diet without any restrictions. Thus, the FOIS in the valleculae means pooling up to the free edge of the
was used as a descriptive diet variable in this study. During epiglottis. For pyriform sinus pooling, severe pooling was
the FEES examination, two liquid bolus consistencies were up to the level of the arytenoids. Aspiration was defined as
administered. Patients were offered three trials of thin liquid bolus passing below the level of the vocal folds entering the
followed by three trials of thick liquid. Each trial contained trachea. Bolus on the true vocal folds secondarily leaking
10 cc of water (thin liquid) or applesauce (One 2 f­ ruit®) in the trachea was also classified as aspiration. Therefore,
(hereafter ‘thick liquid’) dyed with five percent methylene bolus in and below the anterior commissure was scored as
blue as described in previous papers [19–21]. The viscosities aspiration. These FEES outcome variables were described
(measured at 25 degrees Celsius 50 s−1 of shear rate) of the in previous studies and are presented in the supplementary
thin and thick liquid boluses were 1 mPa s and 1200 mPa s, material (Table S1) [20, 21]. Prior to data collection, two
respectively. Furthermore, during the flow test thick liquid experts received consensus training on the interpretation of
met the descriptive criteria for ‘moderately thick’ according the ordinal FEES variables. This is a standardized proce-
to the International Dysphagia Diet Standardisation Initia- dure for each new study containing visuoperceptual assess-
tive (IDDSI) [22]. For safety concerns (risk of severe aspira- ment tools for OD. The protocol of this training has been
tion), some liquid bolus consistencies were not administered described in previous studies [19, 21]. Both observers were
to all patients. Therefore, only subjects who had at least one blinded to the identity and medical history of the patient and
trial with thin liquid or thick liquid were included in the to each other’s ratings (independent rating). The swallow
study. The tip of the flexible fiberoptic endoscope Pentax trials were scored in randomized order at varying speeds
FNL-10RP3 (Pentax Canada, Mississauga, Ontario, Canada) (slow motion, normal, and up to frame-by-frame). To obtain
was positioned just above the epiglottis in the ‘high position’ intraobserver agreement, each observer performed repeated
[18]. FEES images were obtained using a Xion SD camera, measurements of all visuoperceptual FEES variables. More-
XionEndoSTROB E camera control unit (PAL 25 fps), and over, observers were advised to limit the duration of the
Matrix DS datastation with DIVAS software (Xion Medical, measurement sessions (maximum of two hours per session)
Berlin, Germany). The images were recorded on a DVD at to avoid fatigue-related bias.
30 frames per second. Neither a nasal vasoconstrictor nor
a topical anesthetic was administered to the nasal mucosa. Statistical Analysis

FEES Outcome Variables Descriptive statistics were reported in terms of means with
standard deviations (SDs) for numerical variables and
For each FEES swallow trial, three visuoperceptual ordi- number (percentage) for categorical variables. The score
nal variables were scored: postswallow vallecular pooling, indicating more severe impairment of each FEES variable,
postswallow pyriform sinus pooling, and aspiration [20, dependent on liquid bolus consistency (thin or thick liq-
21]. The term ‘pooling’ was defined as the amount of bolus uid), was used for statistical analysis. Where appropriate,
remaining in the valleculae and/or pyriform sinuses after a Chi-square test or Fisher’s exact test was used to analyze
spontaneous clearing swallows. No distinction was made whether the proportions of events (aspiration) were dif-
between right- and left-sided pooling. Postswallow pooling ferent for various amounts of pooling. Logistic regression
was evaluated after the last swallowing of the same bolus, analysis was performed to further explore the association
i.e., after the last piecemeal deglutition swallow. Three- between pooling and aspiration. Correction for pooling in
point ordinal scales (range 0–2) were used to capture pool- the other location (pyriform sinuses versus valleculae) was
ing severity. The categorical rating scale comprises three performed to determine whether pooling location was asso-
levels of pooling severity: no pooling (0), mild-to-moderate ciated with aspiration, independent of pooling in the other
pooling (1), and severe pooling (2). The description of each location. The analysis was also adjusted for the influence
ordinal level of the severity of pooling is based on the per- of tumor stage (T3–4 vs. T1–2), tumor location (pharynx
ceptual judgment of the amount of bolus in relation to the tumor versus non-pharynx tumor), and cancer treatment
size of the valleculae and/or pyriform sinuses. Postswallow (only radiotherapy, only surgery, or multimodality treat-
vallecular pooling was scored as no pooling (‘0’), mild-to- ment). Multimodality treatment refers to a combination of
moderate pooling (‘1’: filling of less than 50% of the val- (primary or salvage) surgery, (neo)adjuvant radiotherapy,
leculae), or severe pooling (‘2’: filling of more than 50% of and/or chemotherapy [23]. Due to the limited number of

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 S. R. Simon et al.: Association Between Pharyngeal Pooling and Aspiration

events (aspiration) and nonevents (no aspiration), it was not Table 1  Frequency distributions of HNC patient characteristics (total
possible to adjust for all three factors simultaneously, and number of patients = 90)
thus, these factors were included in the analysis separately. Characteristics Number of
Furthermore, the effect of tumor stage, tumor location, or patients (%)
cancer treatment on aspiration was determined. A two-sided Age distribution (N = 90)
p value ≤ 0.05 was considered statistically significant. For < 60 years 22 (24.4)
each visuoperceptual ordinal FEES variable, the inter- and ≥ 60 years 68 (75.6)
intraobserver agreement levels were calculated using linear Length of time since completion of HNC treatment (N = 89)
weighted Kappa coefficient [24]. All statistical analyses were < 5 years after treatment 62 (69.7)
performed using IBM SPSS Statistics for Windows, version > 5 years after treatment 27 (30.3)
23.0 (IBM, Armonk, NY). T classification (N = 75)
T1 17 (22.7)
T2 25 (33.3)
Results T3 13 (17.3)
T4 20 (26.7)
Participants N classification (N = 75)
N0 37 (49.3)
Ninety patients (81.1% men) were included in the study. N1 11 (14.7)
The mean age of the patients was 65.9 years (SD 10.8). All N2 25 (33.3)
patients reported OD complaints. Patients’ characteristics N3 2 (2.7)
including TNM classification, tumor location, oncologic M classification (N = 75)
treatment, and FOIS score are presented in Table 1. Pharynx M0 75 (100)
(51.1%) and larynx (26.1%) were the most common tumor Tumor location (N = 88)
sites. Within the group of patients with pharyngeal cancer, Pharynx 45 (51.1)
oropharynx was the most common tumor location (60%). Larynx 23 (26.1)
Squamous cell carcinoma of the head and neck was the most Oral cavity 11 (12.5)
frequent type of cancer (76.7%). The majority of the patients Other ­locationa 9 (10.2)
(88.8%) underwent radiotherapy as single modality or part Treatment (N = 89)
of multimodality treatment (Table 1). Fourteen patients Definitive radiotherapy 37 (41.6)
(16.1%) underwent a tracheotomy. The mean score of the Surgery 10 (11.2)
FOIS was 4.7 (SD 1.8). Seventy-six patients underwent Surgery and adjuvant radio(chemo)therapy 26 (29.2)
the entire FEES examination protocol. For safety concerns Definitive radiochemotherapy 16 (18)
(risk of severe aspiration), 14 patients did not receive the Tracheotomy (N = 87)
entire FEES protocol (3 × 10 cc thin, 3 × 10 cc thick liquid): Tracheotomy 14 (16.1)
3 patients only received thin liquid, and 11 patients only No tracheotomy 73 (83.9)
received thick liquid. FOIS (N = 88)
Level 1 8 (9.1)
Observer Agreement Level 2 9 (10.2)
Level 3 1 (1.1)
The interobserver and intraobserver agreement levels Level 4 5 (5.7)
were sufficient for all FEES variables (all Kappa coeffi- Level 5 38 (43.1)
cients ≥ 0.71, indicating substantial to almost perfect agree- Level 6 14 (15.9)
ment) (Table S2 in supplementary material). Level 7 13 (14.8)

Postswallow Vallecular Pooling HNC head and neck cancer; FOIS functional oral intake scale
a
Tumor sites including the nasal cavity or paranasal sinuses are
reported as ‘Other location’
Thin Liquid Bolus Consistency

Postswallow vallecular pooling of thin liquid bolus con- vallecular pooling aspirated. ‘Mild-to-moderate vallecular
sistency occurred in 39 (51.3%) patients: mild-to-mod- pooling’ compared to ‘no pooling,’ was not significantly
erate and severe vallecular pooling were observed in 24 associated with aspiration (OR 1.94, 95% CI 0.69, 5.51,
(31.6%) and 15 (19.7%) patients, respectively (Table 2). p = 0.212) (Table 3). However, ‘severe vallecular pooling’
Twenty-four (61.5%) of the patients showing postswallow compared to ‘no pooling’ was significantly associated with

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S. R. Simon et al.: Association Between Pharyngeal Pooling and Aspiration

Table 2  Frequency distribution Pooling location and Presence of ­poolinga Aspiration in patients Aspiration in patients who
of the occurrence of liquid bolus consistency N (%) who presented pooling did not present pooling
postswallow pharyngeal pooling N (%) N (%)
and aspiration (total number of
patients = 90) Valleculae
Thin liquid (N = 76) 39 (51.3) 24 (61.5) 14 (37.8)
Thick liquid (N = 79) 69 (87.3) 22 (31.9) 4 (40.0)
Pyriform sinuses
Thin liquid (N = 77) 26 (33.8) 17 (65.4) 22 (43.1)
Thick liquid (N = 80) 38 (47.5) 20 (52.6) 8 (19.0)

N number of patients
a
Presence of postswallow pooling is defined as the presence of mild-to-moderate pooling and/or severe
pooling

Table 3  Association between aspiration and postswallow vallecular or pyriform sinus pooling
Unadjusteda Adjusted for location of p­ oolingb
Thin liquid Thick liquid Thin liquid Thick liquid
OR (95% CI) p-value OR (95% CI) p-value OR (95% CI) p-value OR (95% CI) p-value

Postswallow vallecular pooling

Mild-to-moderate pool- 1.94 (0.69, 5.51) 0.212 0.21 (0.04, 1.11) 0.066 1.39 (0.44, 4.35) 0.572 0.18 (0.03, 1.05) 0.056
ing versus no pooling
Severe pooling versus no 4.52 (1.20, 16.97) 0.026* 1.42 (0.34, 5.88) 0.628 2.58 (0.56, 11.91) 0.226 0.80 (0.17, 3.78) 0.781
pooling
Severe pooling versus 2.33 (0.58, 9.43) 0.236 6.62 (1.94, 22.73) 0.003* 1.86 (0.41, 8.33) 0.420 4.51 (1.17, 17.54) 0.029*
mild-to-moderate
pooling
Postswallow pyriform sinus pooling
Mild-to-moderate pool- 1.13 (0.33, 3.84) 0.845 4.25 (0.87, 20.75) 0.074 0.92 (0.25, 3.42) 0.895 5.87 (1.00, 34.41) 0.05004
ing versus no pooling
Severe pooling versus no 7.25 (1.46, 36.10) 0.016* 4.86 (1.70, 13.91) 0.003* 4.78 (0.80, 28.35) 0.086 3.44 (1.03, 11.47) 0.044*
pooling
Severe pooling versus 6.41 (0.99, 41.67) 0.0501 1.14 (0.24, 5.44) 0.867 5.21 (0.78, 34.48) 0.089 0.59 (0.10, 3.34) 0.548
mild-to-moderate
pooling

OR odds ratio, CI confidence interval

a
Logistic regression analysis, without adjustment for other variables
b
Logistic regression analysis, with adjustment for pooling in the other location
*Significance at p ≤ 0.05

aspiration (OR 4.52, 95% CI 1.20, 16.97, p = 0.026). The Thick Liquid Bolus Consistency
effect of ‘severe vallecular pooling’ compared to ‘mild-to-
moderate pooling’ on aspiration was not significant (OR In 69 (87.3%) patients, postswallow vallecular pooling of
2.33, 95% CI 0.58, 9.43, p = 0.236). Correction for pooling thick liquid bolus consistency was observed and was scored
in the other location was performed to determine whether as mild-to-moderate and severe pooling in 32 (40.5%) and 37
a certain pooling location was associated with aspiration, (46.8%) patients, respectively (Table 2). Aspiration occurred
independent of pooling in the other location. The effect of in 22 (31.9%) of the patients showing postswallow vallecular
‘severe vallecular pooling’ compared to ‘no pooling’ on pooling. The analysis regarding amount of pooling in the
aspiration appeared not significant (OR 2.58, 95% CI 0.56, valleculae showed that, when compared to ‘no vallecular
11.91, p = 0.226) after this correction (pooling in pyriform pooling,’ both ‘mild-to-moderate pooling’ (OR 0.21, 95% CI
sinuses). Similar results were seen after correction for 0.04, 1.11, p = 0.066) and ‘severe pooling’ (OR 1.42, 95%
tumor stage, tumor location, or type of cancer treatment. CI 0.34, 5.88, p = 0.628) were not significantly associated

13
 S. R. Simon et al.: Association Between Pharyngeal Pooling and Aspiration

with aspiration (Table 3). However, the effect of ‘severe val- ‘mild-to-moderate pooling’ on aspiration was not signifi-
lecular pooling’ compared to ‘mild-to-moderate pooling’ on cant (OR 1.14, 95% CI 0.24, 5.44, p = 0.867). Similar results
aspiration was significant (OR 6.62, 95% CI 1.94, 22.73, were seen after correction for pooling in the other location,
p = 0.003). Similar results were seen after correction for and after additional correction for tumor stage, tumor loca-
pooling location, and after additional correction for tumor tion, or type of cancer treatment.
stage, tumor location, or type of cancer treatment.
Effect of Tumor Stage, Tumor Location, or Cancer
Postswallow Pyriform Sinus Pooling Treatment on Aspiration After Correction
for Postswallow Pooling in Both Locations
Thin Liquid Bolus Consistency
After correction for postswallow pooling in valleculae and
Postswallow pyriform sinus pooling of thin liquid bolus pyriform sinuses location, the effect of tumor stage, tumor
consistency occurred in 26 (33.8%) patients: mild-to-mod- location, or cancer treatment on aspiration was determined.
erate and severe pyriform sinus pooling were observed in Both tumor stage (p = 0.764) and tumor location
13 (16.9%) and 13 (16.9%) patients, respectively (Table 2). (p = 0.470) had no significant effect on aspiration in swal-
Seventeen (65.4%) of the patients showing postswallow lows of thin liquid bolus consistency. However, cancer
pyriform sinus pooling aspirated. ‘Mild-to-moderate pyri- treatment showed a significant effect on aspiration (over-
form sinus pooling’ compared to ‘no pooling,’ was not all p = 0.003). The proportion of patients with aspiration
significantly associated with aspiration (OR 1.13, 95% CI was significantly higher for the group of patients who only
0.33, 3.84, p = 0.845) (Table 3). However, ‘severe pyriform underwent definitive radiotherapy, compared to the group
sinus pooling’ compared to ‘no pooling’ was significantly of patients who received multimodality treatment (OR 7.86,
associated with aspiration (OR 7.25, 95% CI 1.46, 36.10, 95% CI 2.19, 28.23, p = 0.002). The group of patients who
p = 0.016). Although a trend toward significance was seen, underwent surgery exclusively, did not have a significantly
the effect of ‘severe pyriform sinus pooling’ compared to increased proportion of patients with aspiration, compared
‘mild-to-moderate pooling’ on aspiration was not significant to the group of patients who received multimodality treat-
(OR 6.41, 95% CI 0.99, 41.67, p = 0.0501). After correction ment (OR 0.79, 95% CI 0.12, 5.07, p = 0.800). Finally, tumor
for pooling in the other location (valleculae), the effect of stage, tumor location, and cancer treatment had no signifi-
‘severe pyriform sinus pooling’ compared to both ‘no pool- cant effect on aspiration in swallows of thick liquid bolus
ing’ (OR 4.78, 95% CI 0.80, 28.35, p = 0.086) and ‘mild-to- consistency (all p-values ≥ 0.209).
moderate pooling’ (OR 5.21, 95% CI 0.78, 34.48, p = 0.089)
on aspiration was not found to be significant. Similar results
were seen following additional correction for tumor stage Discussion
or tumor location. An exception was found after correction
for type of cancer treatment. The effect of ‘severe pyriform In this study, we investigated the relationship between post-
sinus pooling, compared to both ‘no pooling’ (OR 9.99, 95% swallow pharyngeal pooling and aspiration in dysphagic
CI 1.44, 64.47, p = 0.020) and ‘mild-to-moderate pooling’ HNC patients using FEES. Furthermore, we analyzed the
(OR 11.24, 95% CI 1.37, 90.91, p = 0.024), on aspiration was association between tumor stage, tumor location, and cancer
found to be significant. treatment on the one hand, and aspiration on the other hand.
The results of our study showed that location, liquid bolus
Thick Liquid Bolus Consistency consistency, and amount of postswallow pharyngeal pooling
have an influence on the probability of aspiration. ‘Severe
Postswallow pyriform sinus pooling of thick liquid bolus vallecular pooling’ of thick liquid, compared to ‘mild-to-
consistency was observed in 38 (47.5%) patients, which moderate pooling,’ showed a significant association with
was scored as ‘mild-to-moderate’ and ‘severe pooling’ in aspiration, independent of the presence of pooling in the
8 (10%) and 30 (37.5%) patients, respectively (Table 2). pyriform sinuses. However, no significant association was
Aspiration occurred in 20 (52.6%) of the patients showing found between ‘severe vallecular pooling’ of thick liquid
pyriform sinus pooling. ‘Mild-to-moderate pyriform sinus versus absence of pooling and aspiration. This outcome
pooling’ compared to ‘no pooling’ was not significantly is not what would be expected in clinical practice, and no
associated with aspiration (OR 4.25, 95% CI 0.87, 20.75, clear explanation was found for it. It would be interesting
p = 0.074) (Table 3). However, the effect of ‘severe pyri- to replicate this study with a larger sample size to verify if
form sinus pooling’ compared to ‘no pooling’ on aspiration the association might change. Whereas, severe vallecular
was significant (OR 4.86, 95% CI 1.70, 13.91, p = 0.003). pooling of thin liquid, compared to the absence of pooling,
The effect of ‘severe pyriform sinus pooling’ compared to was only significantly associated with aspiration if there

13
S. R. Simon et al.: Association Between Pharyngeal Pooling and Aspiration

was also pooling in the pyriform sinuses. This finding may esophagus and may contribute to the occurrence of bolus
be explained by the greater distance between the valleculae overflow from the pyriform sinuses into the laryngeal ves-
and laryngeal vestibule, compared to the anatomic position tibule [31]. More than 80% of the patients in our study
of the pyriform sinuses relative to the laryngeal vestibule received radiotherapy (single or multimodality treatment).
[25]. As the bolus may spill from the lateral parts of the Ku et al. also found a significant association between posts-
valleculae, the overflow of the bolus from the valleculae wallow pyriform sinus pooling and aspiration assessed dur-
directly into the laryngeal vestibule seems less likely to hap- ing FEES in dysphagic patients with nasopharyngeal car-
pen. The epiglottis might play an additional role as a barrier cinoma [11]. Other studies using VFSS mainly in patients
between the valleculae and laryngeal vestibule, even though with neurogenic OD did not show any association between
oncologic treatment or tumor location (oropharynx, supra- pyriform sinus pooling and aspiration [16, 27]. However,
glottis) in HNC patients may impair the epiglottic function some studies reported that the risk of aspiration increased
due to fibrosis, malformation, and tissue destruction [26]. with the increasing amounts of pharyngeal pooling [27, 32].
Consequently, in the case of severe vallecular pooling, this Likewise, our results showed that an increasing amount of
epiglottis barrier function may fail. Also the phenomena of postswallow pooling in the pyriform sinuses significantly
pooling in both locations (pyriform sinuses and valleculae) increased the incidence of aspiration in HNC patients.
probably indicate a more severe swallowing impairment It was hypothesized that the type of treatment may con-
with an increased risk of aspiration [27]. Previous studies by tribute to the occurrence of postswallow pharyngeal pooling
other authors demonstrated a significant association between and/or aspiration as oncologic treatment can cause impaired
vallecular pooling and aspiration [13, 16, 27]; however, most pharyngeal contraction and laryngopharyngeal motorsen-
studies included mainly non-oncological patients [16, 27]. sory deficits due to fibrosis and postradiation neuropathy
Considerable heterogeneity exists across studies making [6]. Other factors, including an advanced tumor stage, were
comparisons difficult, especially regarding the methodology thought to strengthen the association between postswallow
and study population, as the majority of patients showed pharyngeal pooling and aspiration. However, in the present
neurogenic OD [16, 27]. Only one study included patients study, the association between postswallow pharyngeal pool-
with HNC [13]. Moreover, in previous studies the swallow- ing and aspiration did not change after correcting for tumor
ing function was evaluated with a different assessment tool stage, tumor location, or type of cancer treatment, with the
(VFSS), which may influence the results, considering that exception of a significant association between ‘severe pyri-
FEES may yield more severe scores for both pooling and form sinus pooling’ of thin liquid and aspiration after cor-
penetration/aspiration, when compared to VFSS [28, 29]. rection for type of cancer treatment. The fact that an asso-
Furthermore, nonstandardized bolus consistencies and/or ciation between tumor stage and pooling or aspiration was
varying volumes were administered across these studies [13, not found might be a result of the small sample size: per-
16] and diverse rating scales for pharyngeal pooling were haps an association would have been found if more patients
applied [16, 30]. were included in the study. The distribution of tumor stage
In the current study, we found a significant association among the included patients (i.e., 42 patients with T1 or T2
between severe pyriform sinus pooling versus the absence stage versus 33 patients with T3 or T4 stage) is considered
of pooling and aspiration of thin liquid, without correction fairly equal. A more elaborate statistical analysis, including
for vallecular pooling in the statistical model. This finding detailed group stratification for all (separate) tumor stages,
may be related to the thin and watery nature of the boluses might have led to different results. However, the present
which can very quickly flow, but may not apply for thicker or sample size was too small to allow statistical pooling.
solid boluses that stick and clump. However, after correction Additionally, our results indicated that the occurrence of
for vallecular pooling in the regression model no signifi- aspiration of thin liquid is influenced by cancer treatment,
cant association was found between severe pyriform sinus whereby patients who underwent definitive radiotherapy
pooling versus the absence of pooling and aspiration of thin as a single modality treatment demonstrate significantly
liquid. In the current study, the presence of severe versus higher aspiration rates, compared to patients who received
no pyriform sinus pooling of thick liquid was significantly multimodality treatment, which comprises a combination
associated with aspiration, independent of the presence of of (primary or salvage) surgery, (neo)adjuvant radiotherapy
vallecular pooling. This association may be explained by and/or chemotherapy. According to the report of Pearson
the proximity of the pyriform sinuses to the laryngeal vesti- et al., HNC patients treated with radiotherapy demonstrated
bule, facilitating the overflow of the bolus from the pyriform poor swallowing outcomes, including increased aspiration
sinuses into the laryngeal vestibule [25]. Decreased opening and pharyngeal pooling [33]. However, discordant results on
of the UES, which has been previously observed in patients aspiration have been reported in HNC patients too. Several
with HNC treated with (chemo)radiotherapy, impairs the studies found that aspiration was significantly associated
passage of food or liquids from the (hypo)pharynx into the with either tumor stage [4, 13, 34], tumor location [34, 35],

13
 S. R. Simon et al.: Association Between Pharyngeal Pooling and Aspiration

or cancer treatment [13]. In contrast, other studies could not possible to analyze the potential effect of these parameters
demonstrate a significant relation between either tumor stage on the association between pooling and aspiration. However,
[35], tumor location [4, 13], or cancer treatment [4] on the the patient population included was a realistic representation
one hand, and aspiration on the other hand. It has also been of HNC patients consulting the multidisciplinary outpatient
suggested that the presence of aspiration in HNC patients clinic for dysphagic complaints, which gives insight into
is affected by the type of cancer treatment (surgery, chemo- the overall severity of swallowing impairment in this group.
therapy, or radiotherapy), rather than by tumor location [13]. We hope to investigate these factors in a larger sample size
Our study investigated the potential association between in the future.
postswallow pharyngeal pooling and aspiration using FEES
in dysphagic HNC patients. However, it is unknown whether
the association between postswallow pyriform sinus pooling
Conclusion
and aspiration represents a high co-occurrence rate, or a causal
association. Patients who showed significant pooling during
Location (valleculae versus pyriform sinuses), liquid bolus
FEES may not present aspiration during the examination, but
consistency (thin versus thick liquid), and amount of post-
they may aspirate after the examination or at any time, when
swallow pharyngeal pooling (no pooling, mild/moderate
they are eating at home in their daily habitat [19]. In fact, FEES
pooling, severe pooling) seem to have an influence on the
with its standardized protocols is only a short observation of
probability of aspiration. Severe versus mild-to-moderate
a complex swallowing process, and therefore it is not always
postswallow vallecular pooling of thick liquid was signifi-
a realistic representation of daily swallowing. In a nonclinical
cantly associated to aspiration in HNC patients with OD,
setting, multiple factors may affect the swallowing mechanism
independent of the presence of pyriform sinus pooling,
such as fatigue, increased complexity of feeding in terms of
tumor stage, tumor location, or type of cancer treatment.
various bolus consistencies, and diverse eating behaviors and
Furthermore, this study showed a significant association
postures. Previous research in patients with OD showed that
between severe postswallow pyriform sinus pooling of thick
the risk of aspiration can be underestimated when a limited
liquid and aspiration. This association was independent of
number of swallow trials is performed during FEES [19].
the presence of vallecular pooling, tumor stage, tumor loca-
Based on our results, we assumed that patients presenting
tion, or cancer treatment. Based on these findings, identifica-
severe pyriform sinus pooling of thick liquid are more likely
tion of location and amount of pooling during FEES evalu-
to present aspiration, compared to patients who do not present
ation should be carefully considered, even in the absence of
pooling in the pyriform sinuses. Thus, pyriform sinus pooling
aspiration during the examination.
in HNC patients is not only a marker of impaired swallow effi-
ciency but was also associated with impaired swallow safety
(aspiration). Based on these findings, even when aspiration is
Compliance with Ethical Standards
not observed during a FEES examination, it is presumed that
severe pyriform sinus pooling could be predictive for or associ- Conflict of interest The authors declare that they have no conflict of
ated with aspiration that may or may not have been visualized. interest.
On these grounds, we suggest to pay specific attention to the
presence of postswallow pharyngeal pooling during the swal- Ethical Approval Informed consent was obtained from all patients in
daily clinical practice. The study protocol is classified as non-WMO
lowing assessment, in order to estimate the severity of OD and dutiful according to the Dutch Medical Research Human Subjects Act
to design an appropriate OD management plan. (http://www.ccmo.nl/en/non-wmo-resea​rch) and anonymized patient
data were used.

Limitations of the Study Open Access This article is distributed under the terms of the Creative
Commons Attribution 4.0 International License (http://creat​iveco​mmons​.
Our study has some limitations. Solid food boluses were not org/licen​ses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the
examined in the present study. In some HNC patients, the original author(s) and the source, provide a link to the Creative Com-
pyriform sinuses may be occluded from edema, fibrosis, and/ mons license, and indicate if changes were made.
or surgical changes. The cavity size of the pyriform sinuses
could also be a determining factor in the risk analysis of
aspiration, as well as the subjective visuoperceptual assess-
ment of the amount of pooling. Moreover, the sample size References
was too small to allow detailed group stratification for all
1. Govender R, Smith CH, Taylor SA, Barratt H, Gardner B. Swal-
tumor locations, TNM classifications, and all single or com- lowing interventions for the treatment of dysphagia after head and
bined oncologic treatment modalities. Therefore, it was not neck cancer: a systematic review of behavioural strategies used to

13
S. R. Simon et al.: Association Between Pharyngeal Pooling and Aspiration

promote patient adherence to swallowing exercises. BMC Cancer. 17. Edge SB, American Joint Committee on Cancer., American Can-
2017;17(1):43. https​://doi.org/10.1186/s1288​5-016-2990-x. cer Society. AJCC cancer staging handbook: from the AJCC can-
2. Jiang N, Zhang LJ, Li LY, Zhao Y, Eisele DW. Risk factors for late cer staging manual. 7th ed. New York: Springer; 2010.
dysphagia after (chemo)radiotherapy for head and neck cancer: a 18. Langmore SE, Schatz K, Olson N. Endoscopic and videofluoro-
systematic methodological review. Head Neck. 2016;38(5):792– scopic evaluations of swallowing and aspiration. Ann Otol Rhi-
800. https​://doi.org/10.1002/hed.23963​. nol Laryngol. 1991;100(8):678–81. https:​ //doi.org/10.1177/00034​
3. Schindler A, Denaro N, Russi EG, Pizzorni N, Bossi P, Merlotti 89491​10000​815.
A, Spadola Bissetti M, Numico G, Gava A, Orlandi E, Caspiani O, 19. Baijens LW, Speyer R, Pilz W, Roodenburg N. FEES protocol
Buglione M, Alterio D, Bacigalupo A, De Sanctis V, Pavanato G, derived estimates of sensitivity: aspiration in dysphagic patients.
Ripamonti C, Merlano MC, Licitra L, Sanguineti G, Langendijk Dysphagia. 2014;29(5):583–90. https​://doi.org/10.1007/s0045​
JA, Murphy B. Dysphagia in head and neck cancer patients treated 5-014-9549-2.
with radiotherapy and systemic therapies: literature review and 20. Florie M, Baijens L, Kremer B, Kross K, Lacko M, Verhees F,
consensus. Crit Rev Oncol Hematol. 2015;96(2):372–84. https​:// Winkens B. Relationship between swallow-specific quality of life
doi.org/10.1016/j.critr​evonc​.2015.06.005. and fiber-optic endoscopic evaluation of swallowing findings in
4. Campbell BH, Spinelli K, Marbella AM, Myers KB, Kuhn JC, patients with head and neck cancer. Head Neck. 2016;38(Suppl
Layde PM. Aspiration, weight loss, and quality of life in head 1):E1848–56. https​://doi.org/10.1002/hed.24333​.
and neck cancer survivors. Arch Otolaryngol Head Neck Surg. 21. Pilz W, Vanbelle S, Kremer B, van Hooren MR, van Becelaere
2004;130(9):1100–3. https:​ //doi.org/10.1001/archot​ ol.130.9.1100. T, Roodenburg N, Baijens LW. Observers’ agreement on meas-
5. García-Peris P, Parón L, Velasco C, de la Cuerda C, Camblor M, urements in fiberoptic endoscopic evaluation of swallowing.
Bretón I, Herencia H, Verdaguer J, Navarro C, Clave P. Long-term Dysphagia. 2016;31(2):180–7. https​://doi.org/10.1007/s0045​
prevalence of oropharyngeal dysphagia in head and neck cancer 5-015-9673-7.
patients: impact on quality of life. Clin Nutr. 2007;26(6):710–7. 22. Lam P, et al. Complete IDDSI framework detailed definitions.
https​://doi.org/10.1016/j.clnu.2007.08.006. International Dysphagia Diet Standardisation Initiative. Br J Neu-
6. Hutcheson KA, Lewin JS, Barringer DA, Lisec A, Gunn rosci Nurs. 2017;13:S18–26.
GB, Moore MW, Holsinger FC. Late dysphagia after radi- 23. Sarris EG, Harrington KJ, Saif MW, Syrigos KN. Multimodal
otherapy-based treatment of head and neck cancer. Cancer. treatment strategies for elderly patients with head and neck cancer.
2012;118(23):5793–9. https​://doi.org/10.1002/cncr.27631​. Cancer Treat Rev. 2014;40(3):465–75. https​://doi.org/10.1016/j.
7. Crary MA, Mann GD, Groher ME. Initial psychometric assess- ctrv.2013.10.007.
ment of a functional oral intake scale for dysphagia in stroke 24. Landis JR, Koch GG. The measurement of observer agreement
patients. Arch Phys Med Rehabil. 2005;86(8):1516–20. https​:// for categorical data. Biometrics. 1977;33(1):159–74.
doi.org/10.1016/j.apmr.2004.11.049. 25. Sobotta J, Putz R, Pabst R, Putz R. Sobotta atlas of human anat-
8. Hiss SG, Postma GN. Fiberoptic endoscopic evaluation of omy: head, neck, upper limb, thorax, abdomen, pelvis, lower limb.
swallowing. Laryngoscope. 2003;113(8):1386–93. https​://doi. 14th ed. Munchen: Urban & Fischer/Elsevier; 2008.
org/10.1097/00005​537-20030​8000-00023​. 26. Bleier BS, Levine MS, Mick R, Rubesin SE, Sack SZ, McKinney
9. Langmore SE. Endoscopic evaluation and treatment of swallowing K, Mirza N. Dysphagia after chemoradiation: analysis by modified
disorders. New York: Thieme; 2001. barium swallow. Ann Otol Rhinol Laryngol. 2007;116(11):837–
10. Langmore SE. History of fiberoptic endoscopic evaluation of 41. https​://doi.org/10.1177/00034​89407​11601​108.
swallowing for evaluation and management of pharyngeal dys- 27. Perlman AL, Booth BM, Grayhack JP. Videofluoroscopic pre-
phagia: changes over the years. Dysphagia. 2017;32(1):27–38. dictors of aspiration in patients with oropharyngeal dysphagia.
https​://doi.org/10.1007/s0045​5-016-9775-x. Dysphagia. 1994;9(2):90–5.
11. Ku PK, Vlantis AC, Leung SF, Lee KY, Cheung DM, Abdullah 28. Kelly AM, Drinnan MJ, Leslie P. Assessing penetration and aspi-
VJ, van Hasselt A, Tong MC. Laryngopharyngeal sensory defi- ration: how do videofluoroscopy and fiberoptic endoscopic evalua-
cits and impaired pharyngeal motor function predict aspiration in tion of swallowing compare? Laryngoscope. 2007;117(10):1723–
patients irradiated for nasopharyngeal carcinoma. Laryngoscope. 7. https​://doi.org/10.1097/MLG.0b013​e3181​23ee6​a.
2010;120(2):223–8. https​://doi.org/10.1002/lary.20701​. 29. Kelly AM, Leslie P, Beale T, Payten C, Drinnan MJ. Fibreop-
12. Wu CH, Hsiao TY, Ko JY, Hsu MM. Dysphagia after radio- tic endoscopic evaluation of swallowing and videofluoroscopy:
therapy: endoscopic examination of swallowing in patients does examination type influence perception of pharyngeal residue
with nasopharyngeal carcinoma. Ann Otol Rhinol Laryngol. severity? Clin Otolaryngol. 2006;31(5):425–32. https​://doi.org/1
2000;109(3):320–5. https​://doi.org/10.1177/00034​89400​10900​ 0.1111/j.1749-4486.2006.01292​.x.
315. 30. Pearson WG Jr, Molfenter SM, Smith ZM, Steele CM. Image-
13. Jung SJ, Kim DY, Joo SY. Rick factors associated with aspira- based measurement of post-swallow residue: the normalized
tion in patients with head and neck cancer. Ann Rehabil Med. residue ratio scale. Dysphagia. 2013;28(2):167–77. https​://doi.
2011;35(6):781–90. https​://doi.org/10.5535/arm.2011.35.6.781. org/10.1007/s0045​5-012-9426-9.
14. Dodds WJ, Logemann JA, Stewart ET. Radiologic assessment 31. Wall LR, Ward EC, Cartmill B, Hill AJ. Physiological changes
of abnormal oral and pharyngeal phases of swallowing. AJR to the swallowing mechanism following (chemo)radiotherapy
Am J Roentgenol. 1990;154(5):965–74. https​://doi.org/10.2214/ for head and neck cancer: a systematic review. Dysphagia.
ajr.154.5.21085​70. 2013;28(4):481–93. https​://doi.org/10.1007/s0045​5-013-9491-8.
15. Eisbruch A, Lyden T, Bradford CR, Dawson LA, Haxer MJ, Miller 32. Eisenhuber E, Schima W, Schober E, Pokieser P, Stadler A,
AE, Teknos TN, Chepeha DB, Hogikyan ND, Terrell JE, Wolf Scharitzer M, Oschatz E. Videofluoroscopic assessment of
GT. Objective assessment of swallowing dysfunction and aspira- patients with dysphagia: pharyngeal retention is a predictive factor
tion after radiation concurrent with chemotherapy for head-and- for aspiration. AJR Am J Roentgenol. 2002;178(2):393–8. https:​ //
neck cancer. Int J Radiat Oncol Biol Phys. 2002;53(1):23–8. doi.org/10.2214/ajr.178.2.17803​93.
16. Molfenter SM, Steele CM. The relationship between residue and 33. Pearson WG Jr, Davidoff AA, Smith ZM, Adams DE, Langmore
aspiration on the subsequent swallow: an application of the nor- SE. Impaired swallowing mechanics of post radiation therapy
malized residue ratio scale. Dysphagia. 2013;28(4):494–500. https​ head and neck cancer patients: a retrospective videofluoroscopic
://doi.org/10.1007/s0045​5-013-9459-8.

13
 S. R. Simon et al.: Association Between Pharyngeal Pooling and Aspiration

study. World J Radiol. 2016;8(2):192–9. https​://doi.org/10.4329/ Sorina R. Simon MD

wjr.v8.i2.192.
34. Starmer H, Gourin C, Lua LL, Burkhead L. Pretreatment swallow- Michelle Florie MD
ing assessment in head and neck cancer patients. Laryngoscope.
2011;121(6):1208–11. https​://doi.org/10.1002/lary.21800​. Walmari Pilz SLP, PhD
35. Stenson KM, MacCracken E, List M, Haraf DJ, Brockstein B,
Weichselbaum R, Vokes EE. Swallowing function in patients with Bjorn Winkens PhD
head and neck cancer prior to treatment. Arch Otolaryngol Head
Neck Surg. 2000;126(3):371–7. Bernd Kremer MD, PhD

Publisher’s Note Springer Nature remains neutral with regard to Laura W. J. Baijens MD, PhD
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