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Dysphagia DOI 10.1007/s00455-011-9359-8

ORIGINAL ARTICLE

Effects of Carbonated Liquids on Oropharyngeal Swallowing Measures in People with Neurogenic Dysphagia Katerina Sdravou • Margaret Walshe Lukas Dagdilelis



Received: 15 January 2011 / Accepted: 19 July 2011 ! Springer Science+Business Media, LLC 2011

Abstract Aspiration is common in adults with neurogenic dysphagia and pharyngeal delay. This can lead to dehydration, malnutrition, and aspiration pneumonia. Diet modifications aimed at reducing thin liquid aspiration are partially successful or unpalatable or both. Carbonated liquids show some potential in influencing swallowing behavior. However, there is a paucity of evidence to support this intervention. This study compares the effects of carbonated thin liquids (CTL) with that of noncarbonated thin liquids (NCTL) on oropharyngeal swallowing in adults with neurogenic dysphagia and examines the palatability of the CTL stimulus. Seventeen people with pharyngeal delay attended for videofluoroscopy (VFSS). Outcome measures were oral transit time (OTT), pharyngeal transit time (PTT), stage transition duration (STD), initiation of the pharyngeal swallow (IPS), penetration-aspiration scale (PENASP), and pharyngeal retention (PR). A modification of Quartermaster Hedonic Scale (AQHS) was employed to assess palatability of the CTL. CTL vs. NCTL significantly decreased penetration and aspiration on 5-ml (P = 0.028) and 10-ml (P = 0.037) swallows. CTL had no significant effect on OTT, PTT, IPS, and PR for any volume of bolus. Only one participant disliked the CTL stimulus. These findings support the hypothesis that oropharyngeal

K. Sdravou ! M. Walshe Department of Clinical Speech & Language Studies, Trinity College Dublin, Dublin 2, Ireland L. Dagdilelis X-ray Department, General Hospital ‘‘G. Papanikolaou’’, Thessaloniki, Greece K. Sdravou (&) Kardia, P.O. Box 161, 57500 Thessaloniki, Greece e-mail: [email protected]

swallowing can be modulated in response to sensory stimuli. Implications for research and clinical practice are discussed. Keywords Deglutition ! Deglutition disorders ! Oropharyngeal dysphagia ! Carbonated liquids ! Sensory stimulation ! Neurogenic dysphagia Oropharyngeal dysphagia occurs in a wide variety of the central nervous system (CNS) disorders, including stroke and traumatic brain injury (TBI) [1–3]. Aspiration is one of the most common symptoms in adults with CNS oropharyngeal dysphagia which may lead to dehydration, malnutrition, and aspiration pneumonia [1, 3, 4]. Adults with CNS disorders are more likely to aspirate thin-consistency liquids, with delayed or absent pharyngeal response being the most prevalent cause of thin liquid aspiration in these populations [1, 4, 5]. Several rehabilitative approaches and compensatory strategies are used to eliminate aspiration. However, issues such as cognitive and communication deficits, poor levels of compliance, and general fatigue limit the potential for dysphagia rehabilitation and highlight the importance of finding compensatory interventions that require few physical and cognitive demands on the part of the person with dysphagia. So far, diet modification, specifically increasing liquid viscosity, has been the most common compensatory strategy for people who aspirate on thin liquid. However, the evidence to support this approach is weak and research has found that people on diets using thickened liquids have a higher incidence of pneumonia and rarely meet their fluid intake requirements [6, 7]. As a compensatory strategy, altering the characteristics of the food bolus, focusing on sensory stimulation to

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modulate the oropharyngeal swallow process, shows some promise. A number of studies have suggested that heightening the sensory input via sensory techniques may be the best approach to managing CNS oropharyngeal dysphagia [8–14]. The provision of increased or specific sensory input to the oropharyngeal receptors might enhance the excitability of the central pathway. Thus, the increase in the activation of the swallowing centers may result in triggering faster or more effective ‘‘patterned responses’’ and reduce aspiration [10, 12, 13]. Compensatory sensory interventions, including modifications of bolus characteristics, have been used with varying success to modify the threshold of the patterned swallow response with the prime goal of eliminating aspiration. Examining the effects of manipulating food characteristics such as taste and chemesthesis on swallowing have not been studied extensively in humans. Oral chemesthesis is the sense of chemical irritation (e.g., cooling, burning, tingling) to common somesthetic receptors elicited by a variety of chemical stimuli, including salts, acids, capsaicin, menthol, and carbonation. Oral chemesthesis is mediated by the trigeminal nerve, which is the main chemosensory pathway along with the glossopharyngeal and the vagus nerve [8, 13, 15–20]. The majority of the research on the effects of chemesthetic stimuli on swallowing has focused on the effects of citric acid [21–23]. These studies provide some evidence to support the positive effects of citric acid on swallowing physiology. The particular stimulus, however, is often unpalatable thus limiting its use as a treatment strategy [21, 22]. In order to identify palatable liquids to use to reduce thin liquid aspiration, some studies examined the effects of carbonation, an acidic chemesthetic stimulus, on swallowing physiology [24–29]. However, these studies provide weak evidence to support or refute the effects of carbonated liquids on the physiology of swallowing. Specifically, Nixon [29] investigated the effects of carbonated versus thin barium liquids on swallowing measures in four groups of adults, three of which had dysphagia using videofluoroscopy (VFSS). The author reported that the first and second groups exhibited significantly decreased oral transit times (OTT), pharyngeal transit times (PTT), pooling, and aspiration with carbonated liquids. However, there were important drawbacks related to this study. Specifically, the participants had dysphagia due to several neurological disorders whereas those with potential lower motor neuron involvement were not specifically excluded. All these conditions, however, might affect sensory receptors which are hypothesized to be triggered by carbonation. Moreover, the formula of the effervescent granules and operational definitions of the temporal measures were not provided, which makes the replication of that study challenging. Additionally, no measurements of

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interrater and intrarater reliability were reported, raising questions regarding the validity of the findings. Newman et al. [28] explored the effects of carbonation on the physiology of swallowing in 24 infants and children with dysphagia. Results showed that carbonated thin liquids (CTL) significantly reduced the incidence of spillover, delayed pharyngeal response, and laryngeal penetration compared to noncarbonated thin liquids (NCTL), although no significant effect was found on aspiration. The authors suggested that the absent effect on aspiration could be due to the small number who aspirated (n = 7) and concluded that carbonation may be a therapeutic option in children with dysphagia. However, the authors did not specify the etiologies of dysphagia. Bulow et al. [24] found that CTL significantly reduced penetration/aspiration into the airways, pharyngeal transit time, and pharyngeal retention when compared to both thin and thickened liquids in 40 adults with thin liquid aspiration. However, the inclusion of participants with non-neurogenic dysphagia and the lack of controls for systematic bias such as randomization of the stimulus order, blinding, or inter/intrarater reliability indicators make the results vulnerable to research bias. Furthermore, the use of arbitrary rating scales for penetration/ aspiration and pharyngeal retention that have not been validated make it difficult to decide on the efficacy of carbonated thin liquids in reducing aspiration. The study, however, highlights the important clinical significance of carbonated liquids and provides support for their use in the dysphagia clinic. Krival [26] examined the effects of CTL compared to NCTL, nectar-like, and honey-like thickened liquids on the physiology of swallowing in 14 adults with dysphagia following stroke. The author found no significant differences in stage transition duration (STD), pharyngeal transit time (PTT), penetration-aspiration (PENASP), pharyngeal retention (PR), and bolus position at the onset of the swallow (BPOS) between carbonated and noncarbonated thin liquids. However, the participants were enrolled in the study regardless of the nature of the oropharyngeal dysphagia. Sensation elicited by carbonation had been theorized to modify the patterned swallowing response and, thus, carbonated liquids were proposed as a sensory intervention to eliminate thin liquid aspiration, but delay in the triggering of the pharyngeal swallow or thin liquid penetration/aspiration was not included in the inclusion criteria of this study. Moreover, the cool temperature of the stimuli not only might stimulate the temperature receptors, it might also inhibit the perception of nociceptive stimulus such as carbonation. Thus, that study inadvertently examined the effect of cool carbonated and cool noncarbonated thin liquid. More recently, Miura et al. [27] examined the effects of taste, carbonation, and cold temperature on the power

K. Sdravou et al.: Effects of Carbonated Liquids

frequency content of swallowing using surface electromyography (sEMG) in healthy subjects. The authors found that taste, carbonation, and cold stimulus have qualitatively different influences in the power frequency content of swallowing on sEMG. According to the authors, the increase in the high-frequency content of swallowing sEMG for the sour and carbonated stimuli is likely to reflect a more organized activation of submental muscle, with more adequate and effective afferent inputs into the nucleus tractus solitarius (NTS) in the brainstem. This area is worthy of further investigation as Steele and Miller [30] suggest in their review of the literature on sensory input mechanisms and their role in swallowing. They hypothesize that the gas in a carbonated bolus may act as both a touch-pressure stimulus and a dynamic taste or chemesthetic stimulus. However, like citric acid, there is a risk that this too may be unpalatable to people with dysphagia. The aim of this study was to investigate the immediate effects of carbonated thin liquids (CTL) compared with noncarbonated thin liquids (NCTL) on oropharyngeal swallowing in adults with central nervous system (CNS) neurogenic dysphagia and delayed swallow response. Second, this study aimed to assess the palatability of the CTL stimulus. Our hypothesis was that CTL influences swallow function by increasing swallow efficiency and reduce the incidence of aspiration in this population.

80 years of age, (2) CNS disorders confirmed by MRI or CT scan, (3) confirmed oropharyngeal dysphagia on clinical bedside examination consistent with the medical diagnosis, (4) ability to tolerate and cooperate with VFSS, (5) confirmed delayed pharyngeal response on NCTL determined by VFSS, and (6) ability to give informed consent, in accordance with ethical guidelines. Individuals with a history of head and neck tumors and/ or with surgery to the head and neck regions and/or with a history of peripheral nervous system diseases were excluded from the study, as these conditions might affect sensory receptors and peripheral nerves. Pregnant women, people who were in a dependent relationship, or who worked with the researcher were also excluded in accordance with ethical guidelines. Thirty-two individuals were eligible for inclusion in the study prior the VFSS. Only 17 people, 5 women and 12 men, met the inclusion criteria (Table 1). All participants were considered to have oropharyngeal dysphagia with associated pulmonary disease. All were outpatients. Participants 7, 8, and 16 had a tracheostomy tube sited in the past but was no longer in situ at the time of the study. Participants varied in time post onset, with those who were 3–60 days post onset considered as acute. Participants who were [60 days post onset were judged to have chronic issues with old dysphagia complaints. Materials

Methodology This was a phase 1 study of treatment effect [31]. Approval from the Ethics Committee of the Scientific Council of the ‘‘G. Papanikolaou’’ Hospital, Thessaloniki, Greece, was obtained at the outset. A crossover design was used and each participant acted as his/her own control. Participants were assessed drinking NCTL and CTL and the results were measured using temporal and descriptive methods. To assess the palatability of the CTL, a simple ordinal scale was used. Participants The G*Power 3 program [32] was used to calculate the appropriate sample size of the participants. Accordingly, for the t test (matched pairs), with an alpha level of 0.05, power of 0.8, and 0.5 effect size, the estimated required sample size was 27 people. The participants were recruited in this study via a convenience sampling strategy. Participants referred by physicians or speech-language pathologists (SLPs) for VFSS at the research site and who met the inclusion criteria were invited to participate in the study. Inclusion criteria were (1) men and women between 18 and

High-density barium sulfate powder (Barilux" HD, Sanochemia Diagnostics GmbH, Germany) mixed with deionized water was the solution used for all stimulus samples. Deionized water was used in order to control for water taste. Barilux HD is routinely used at the research site for VFSS. All the stimuli were composed of 40% weight/volume barium sulfate concentration in order to achieve equivalent radiographic image quality for each swallow. Two types of liquids were prepared: NCTL and CTL. The CTL consisted of 100 ml thin barium liquid mixed with 1.3 g citric acid anhydrous (Sigma-Aldrich Laborchemikalien GmbH, Germany) and 4 g sodium bicarbonate powder (Sigma-Aldrich Chemikals, Austria). The formula for the carbonated stimulus used in the study followed the principle that three molecules of sodium bicarbonate are required to neutralize one molecule of citric acid, resulting in the liberation of carbon dioxide [33] and the ratio of sodium bicarbonate/barium liquid of the carbonated stimulus that Bulow et al. [24] used. This formula was tested at room temperature (20–25#C) in the laboratory of the Technological Institute of Thessaloniki and was found to be effective in terms of producing carbon dioxide.

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K. Sdravou et al.: Effects of Carbonated Liquids Table 1 Participants’ characteristics (N = 17) Participant identification code

Age (years)

Gender

Neurological diagnosis

No. of days from onset of dysphagia

P1

74

F

Ischemic CVA

P2

71

M

Hemorrhagic CVA

143

No

P3

80

M

Ischemic CVA

3

No

P4

70

L

Ischemic CVA

252

P5

53

L

Right ‘‘Wallenberg Syndrome’’

P6

70

L

Hemorrhagic CVA

P7 P8

22 23

M F

TBI TBI

P9

79

L

Multiple ischemic CVAs

P10

69

L

Ischemic CVA

P11

49

F

Hemorrhagic CVA

P12

80

F

Ischemic CVA

P13

55

M

TBI

238

P14

52

L

Hemorrhagic CVA

343

P15

70

M

Ischemic CVA

P16

42

M

SBI

P17

78

F

Ischemic CVA

60

5 156 1,025 1,322 284 48 3,527 5

20

Tube feeding at time of assessment and tube type Yes, nasogastric (NG)

Yes, PEG Yes, gastrostomy (PEG) No No Yes, PEG No Yes, NG Yes, PEG Yes, NG No No Yes, NG

3,664

No

154

No

Table 2 Definitions of the temporal outcome measures Temporal measure

Definition

Oral transit time (OTT)

Interval from onset of the tongue propelling the bolus posteriorly until the bolus head passes the base of the tongue

Pharyngeal transit time (PTT)

Interval from the bolus head passing the base of the tongue until the bolus tail passes through the cricopharyngeal sphincter

Stage transition duration (STD)

Interval from the bolus head passing the base of the tongue until the beginning of maximum anterior hyoid excursion

Outcome Measures VFSS was the instrumental assessment chosen to demonstrate change and measure the effects of the CTL on swallowing. VFSS studies were conducted using Opera T20c (GMM, Italy), computerized fluoroscopic unit. The fluoroscopic images were recorded on a super-VHS videotape recorder (Panasonic NV-HS960 SVHS) with facilities for controlled slow motion and frame-by-frame analysis (25 frames per second). Both temporal [oral transit time (OTT), pharyngeal transit time (PTT) and stage transition duration (STD)] [34–36] (Table 2) and descriptive [initiation of the pharyngeal swallow (IPS), penetration-aspiration scale (PENASP), and pharyngeal retention (PR)] [37–39] (Table 3) measures of bolus flow were selected to examine the effects of carbonation on swallowing. The Quartermaster Hedonic Scale [40] was adapted and used to investigate the palatability of the CTL. The adaptation of the original scale was made in order to simplify

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the scale to facilitate participant rating (Table 4). Additionally, a meta-analysis on the optimal length of rating scales [41] has shown that five-point scales produced very reliable results and the addition of a midpoint, indicating a neutral position, increased reliability. Procedure A radiologist and the senior author (KS) performed the VFSS studies. During the VFSS, participants were instructed to sit in an upright position and were viewed in the lateral projection. The stimuli were prepared prior to each examination while the barium liquid was added to the dry ingredients of the carbonated stimulus just before the swallowing procedure. All stimuli were measured using a graduated syringe and were presented to participants at room temperature (20–25#C) according to the research protocol (Fig. 1). NCTL Thin barium liquid trials were presented in the following sequence: (1) 5-ml spoon to act as ‘‘warm-up’’ for swallowing; (2) 5-ml spoon of NCTL; (3) 10 ml of

K. Sdravou et al.: Effects of Carbonated Liquids Table 3 Definitions of the descriptive outcome measures Descriptive measure

Definition

Initiation of the Pharyngeal 0 = Bolus head at posterior angle of the ramus (first hyoid excursion) Swallow Scale (IPS) 1 = Bolus head at vallecular pit 2 = Bolus head at posterior laryngeal surface of epiglottis 3 = Bolus head at pit of pyriforms 4 = No appreciable initiation at any location Penetration–Aspiration Scale (PENASP)

1 = Material does not enter the airway 2 = Material enters the airway, remains above the vocal folds, and is ejected from the airway 3 = Material enters the airway, remains above the vocal folds, and is not ejected from the airway 4 = Material enters the airway, contacts the vocal folds, and is ejected from the airway 5 = Material enters the airway, contacts the vocal folds, and is not ejected from the airway 6 = Material enters the airway, passes below the vocal folds, and is ejected into the larynx or out of the airway 7 = Material enters the airway, passes below the vocal folds, and is not ejected from the trachea despite effort 8 = Material enters the airway, passes below the vocal folds, and no effort is made to eject

Pharyngeal Retention Scale (PR)

0 = No pharyngeal retention 1 = Mild pharyngeal retention (the level of contrast material in the valleculae or pyriform sinus constituted less than 25% of the height of the structure) 2 = Moderate pharyngeal retention (the level of contrast material constituted between 25 and 50% of the height of the structure) 3 = Severe pharyngeal retention (the level of contrast material constituted more than 50% of the height of the structure).

Table 4 The adapted Quartermaster Hedonic Scale (AQHS) 1

2

3

4

5

Like extremely

Like

Neither like nor dislike

Dislike

Dislike extremely

NCTL offered from a cup; and (4) 25 ml of NCTL selfregulated cup drinking. When a delayed pharyngeal swallow without aspiration occurred in any of these trials, then carbonated thin barium liquids were given with the same sequence (without another warm-up trial). When aspiration occurred in one of the thin liquid trials, the participants

Fig. 1 Research protocol: stimuli presentation

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were given the carbonated liquid trials. The administration of the carbonated liquids continued until aspiration (as viewed on VFSS) occurred. Participants were asked to self-feed, when possible. When required, assistance was provided by a SLP. All participants were told to swallow as they would normally after the administration of the stimuli without keeping the bolus in their mouths in order to stimulate natural swallowing. When the test trials were completed, each participant continued with VFSS according to the routine hospital protocol. After the completion of the VFSS, participants were asked to rate the CTL according to the modified Quartermaster Hedonic Scale (AQHS).

determine whether the CTL had significant effects on the three temporal measures of swallowing (OTT, PTT, STD), a parametric paired-samples t-test (one-tailed) was used because the data were normally distributed. The Wilcoxon matched-pairs signed-ranks test was employed to test possible differences between CTL and NCTL on the three descriptive measures of swallowing (IPS, PENASP, PR) because the data were on an ordinal scale. The v2 test was used to determine whether the participants found the CTL palatable. A probability of 5% was taken to indicate a statistically significant difference with confidence intervals of 95% in all tests.

Preparation of Data for Analysis

Results

The VFSS recordings were analyzed at normal speed, in slow motion, and frame by frame as many times as needed for confident judgment by the first author (KS), who is experienced in VFSS analysis. The rater (KS) was blinded to the liquid type when analyzing the VFSS studies. The first swallow of each trial on each volume was analyzed. In case of aspiration in a subsequent swallow (e.g., the second swallow of the 25 ml CTL), only the particular ‘‘worst’’ swallow and not the first one was analyzed (e.g., the second swallow of 25 ml CTL and the second swallow of 25 ml NCTL). Seventeen participants were given 5 ml of the tested stimuli, 12 were given 10 ml, and 7 proceeded to the 25-ml cup drinking according to the research protocol. Three of the 17 participants were excluded from the OTT analyses as they did not maintain head position during the VFSS and thus did not provide any data for OTT of each volume, but they did provide data for STD.

Statistical analysis demonstrated that CTL vs. NCTL did not significantly reduce OTT of 5 ml [t = 0.629, P = 0.27, mean difference (MD) = 0.61, 95% CI -1.49 to 2.72], OTT of 10 ml (t = 0.951, P = 0.182, MD = -0.97, 95% CI -3.24 to 1.30), and OTT of 25 ml (t = 0.691, P = 0.26, MD = 1.10, 95% CI = -3.00 to 5.22). The effect sizes indicated a small decrease in the duration of 5-ml OTT (d = 0.16), a small increase in the duration of 10-ml OTT (d = 0.29), and a rather moderate decrease in the duration of 25-ml OTT (d = 0.30) in response to CTL vs. NCTL (Table 5). The CTL had no significant effect on PTT of 5 ml (t = 0.986, P = 0.17, MD = 0.28, 95% CI -0.32 to 0.87), PTT of 10 ml (t = 0.783, P = 0.227, MD = 0.48, 95% CI -0.92 to 1.89), and PTT of 25 ml (t = 0.485, P = 0.322, MD = 0.20, 95% CI -0.83 to 1.24). The effect sizes reflected a small reduction in 5-ml PTT (d = 0.25), 10-ml PTT (d = 0.25), and 25-ml PTT (d = 0.19) (Table 6). Patient 11 (P11) was considered an outlier and was excluded from the analysis of PTT of 5 ml, restricting the sample size to 16. P6 and P10 were also atypical cases and were excluded from the analysis of PTT of 10 ml, restricting the size of the sample to 10 people. Likewise, CTL did not significantly reduce STD of 5 ml (t = 1.21, P = 0.12, MD = 0.33, 95% CI -0.25 to 0.91) and STD of 10 ml (t = 0.692, P = 0.253, MD = 0.42, 95% CI -0.95 to 1.79). Again, P11 was considered an outlier and was excluded from the analysis of STD of 5 ml and P6 and P10 were excluded from the analysis of STD of 10 ml. The effect sizes reflected a small decrease in 5-ml STD (d = 0.30) and 10-ml STD (d = 0.22). However, CTL significantly increased STD of 25 ml (t = -2.39, P = 0.031, MD = -0.32, 95% CI -0.66 to 0.024, d = 0.97) (Table 7). P6 was considered to be an outlier and was excluded from the second analysis of STD of 25 ml. The CTL vs. NCTL had no statistically significant effect on IPS of 5-ml (z = 0.302, P = 0.38, one-tailed, r = 0.07)

Measurement of Reliability To control for intrarater reliability, the first author randomly selected and reanalyzed 20% of the VFSS studies (n = 4) 1 week after the initial rating. Results showed an absolute agreement (intraclass correlation coefficient [ICC] = 1) for the descriptive and the temporal measures, indicating strong intrarater reliability. In order to control any subjective bias and to estimate interrater reliability, one SLP, experienced in rating videofluoroscopy measures and who was not involved in the research project, randomly selected 20% (n = 4) of the VFSS studies. This second rater was blinded to the liquid type. ICC values were calculated to be 0.99 for both the descriptive and the temporal variables, suggesting high interrater reliability. Statistical Analysis All data were entered into the Statistical Package for Social Sciences (SPSS) ver. 16 (SPSS, Inc., Chicago, IL). To

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K. Sdravou et al.: Effects of Carbonated Liquids Table 5 OTT of NCTL and CTL of each volume across participants (N = 14)

Table 7 STD of NCTL and CTL of each volume across participants (N = 17)

Participant ID

Participant ID

5-ml STD (s)

10-ml STD (s)

25-ml STD (s)

NCTL

CTL

NCTL

CTL

NCTL

CTL

5-ml OTT (s)

10-ml OTT (s)

25-ml OTT (s)

NCTL

CTL

NCTL

NCTL

CTL

1

0.40

0.52









1

0.44

0.44









2

1.04

0.44









2

0.36

0.36









3 4

1.28 1.68

2.12 0.60

0.68 0.76

0.44 0.72

0.36 –

1.16 –

3 4

0.24 2.96

0.32 1.68

0.28 7.00

0.52 2.64

0.04 –

0.88 –

6

4.08

1.80

0.52

10.16





5

0.00

0.00

0.20

0.40

0.08

0.44

9

0.48

1.56

0.72

0.76





6

3.20

1.36

23.16

0.00





10

1.80

3.52

0.20

3.00

9.52

0.52

7

2.32

3.20









11

13.68

1.32

0.24

0.28





8

1.72

0.48









12

1.08

1.04

0.76

0.56

0.60

0.36

9

0.12

0.00

0.04

0.32





13

0.16

0.32









10

5.04

1.84

2.20

8.72

0.40

0.56

14

1.48

0.88

0.72

2.68

0.48

1.32

11

0.00

9.16

3.36

0.44





15

0.52

4.16

6.48

2.12

1.68

3.00

12

0.12

0.32

0.32

0.32

0.32

0.84

16

0.88

0.76

0.56

0.48

0.84

0.48

13

0.44

0.20









17

0.52

1.44

0.68

1.80





14

0.24

1.48

0.12

0.00

0.00

0.12

15

0.28

0.00

0.00

2.68

2.20

2.12

16

0.12

0.28

0.16

0.08

2.80

0.36

17

1.12

1.48

0.56

0.44





CTL

Table 6 PTT of NCTL and CTL of each volume across participants (N = 17) Participant ID

5-ml PTT (s)

10-ml PTT (s)

25-ml PTT (s)

NCTL

CTL

NCTL

CTL

NCTL

CTL

1

1.08

0.92









2

1.04

1.00









3

0.72

0.88

0.96

0.96

0.64

1.44

4 5

3.80 0.88

2.20 0.84

7.88 1.32

3.24 1.20

– 1.16

– 1.20

6

3.72

1.96

24.04

0.36





7

3.08

3.88









8

2.32

1.00









9

0.64

0.68

0.60

0.80





10

5.56

2.48

2.80

9.32

1.00

1.08

11

0.44

9.80

4.04

1.04





12

0.60

0.84

0.80

0.88

0.88

1.32

13

1.08

0.84









14

0.64

1.96

0.64

0.56

0.52

0.56

15

0.64

1.44

0.56

3.16

2.80

2.60

16

0.80

0.84

0.64

0.68

3.44

0.80

17

1.60

2.00

0.96

1.00





and 25-ml swallows (z = 0.00, P = 0.5, one-tailed). Although there was no significant difference between the 10-ml CTL and 10-ml NCTL in IPS as well (z = 0.954, P = 0.17, one-tailed), the effect size (r = 0.275) reflected a medium decrease in IPS score on 10 ml of CTL (Table 8). CTL significantly reduced PENASP scores of 5-ml (z = 1.901, P = 0.028, one-tailed) and 10-ml swallows (z = 1.786, P = 0.037, one-tailed). Accordingly, the effect

Table 8 IPS scale score for NCTL and CTL of each volume across participants (N = 17) Participant ID

5-ml IPS

10-ml IPS

25-ml STD

NCTL

CTL

NCTL

CTL

NCTL

CTL

1

3

3









2

3

3









3 4

1 3

1 3

3 3

3 3

0 –

1 –

5

0

0

3

2

0

2

6

2

2

3

1





7

3

3









8

3

3









9

1

0

1

2





10

1

2

3

2

3

1

11

0

3

3

3





12

2

3

3

3

3

2

13

2

1









14

3

2

1

0

0

1

15

1

0

0

2

2

1

16

3

3

3

3

3

3

17

1

2

3

1





sizes indicated a large decrease in PENASP scores of 5-ml CTL vs. 5-ml NCTL (r = 0.46) and of 10-ml CTL vs. NCTL (r = 0.51). CTL had no significant effect on PENASP scores of 25 ml with relatively small effect size (z = 0.535, P = 0.29, one-tailed, r = 0.20) (Table 9).

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K. Sdravou et al.: Effects of Carbonated Liquids Table 9 PENASP scale score of NCTL and CTL of each volume across participants (N = 17)

Table 10 PR scale score for NCTL and CTL of each volume across participants (N = 17)

Participant ID 5-ml PENASP

Participant ID

10-ml PENASP

25-ml PENASP

NCTL

CTL

NCTL

CTL

NCTL

CTL

1

8

3









2

7

3









3 4

1 1

1 1

1 2

2 7

1 –

5

1

1

4

2

6

3

1

8

7

8

4



8

8

1

9

1

10

5-ml PR

10-ml PR

25-ml PR

NCTL

CTL

NCTL

CTL

NCTL

CTL

1

0

0









2

2

2









1 –

3 4

1 1

1 1

1 0

1 1

1 –

0 –

1

4

5

2

1

1

2

1

2

1





6

0

0

1

1











7

0

1

















8

1

1









1

8

2





9

1

0

2

0





1

1

1

1

7

7

10

3

2

3

3

3

3

11

1

1

7

1





11

0

0

0

0





12

2

2

2

1

2

1

12

0

0

0

0

0

0

13

7

1









13

0

0









14

1

2

1

1

1

1

14

0

3

3

1

2

2

15

1

3

2

1

1

1

15

1

0

0

1

0

0

16

1

1

2

2

7

1

16

0

1

0

0

0

0

17

1

2

8

3





17

1

0

1

3





No significant difference was found between CTL and NCTL with respect to PR severity of 5-ml swallows (z = 0.302, P = 0.38, one-tailed, r = 0.07), 10-ml swallows (z = 0.107, P = 0.45, one-tailed, r = 0.03) and 25-ml swallows (z = 0.00, P = 0.5, one-tailed) (Table 10). Regarding stimulus palatability, 58.8% (n = 10) of the participants liked or extremely liked CTL, 23.5% (n = 4) were uncertain, and 17.7% (n = 3) of the participants disliked or extremely disliked CTL. Only one of these three people extremely disliked CTL. Statistical analysis showed a marginal nonstatistical difference (v2 = 3.769, P = 0.052), which suggests a tendency of the individuals to like the CTL.

Discussion and Clinical Implications The PENASP scale evaluates depth, response, and clearance of airway invasion to determine severity of dysphagia and the safety of oral intake. Adults without dysphagia have an average PENASP score of 1.12 (range = 1–2.5) [42]. High scores ([4) reflect the severity of bolus aspiration and may represent significant dysphagia. Management of neurogenic dysphagia involves mainly decreasing the risk of aspiration and aspiration pneumonia. As such, the effects of a therapeutic intervention on reducing PENASP scores are of major clinical importance. The CTL compared to the NCTL was found to significantly decrease the PENASP scores of 5-ml and 10-ml swallows, with all the 17 participants drinking 5 ml CTL safely (without

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aspiration) (P = 0.028) and 15 of them drinking 10 ml CTL safely (P = 0.037). While no significant effect of CTL was found on 25-ml cup drinking, 10 people could tolerate cup drinking without aspiration, whereas only 5 of them could drink NCTL without aspiration. These results confirm previous studies that reported significant decreased penetration and aspiration in response to carbonation and to other chemesthetic stimuli [21, 22, 24, 29]. Only Krival [26] reported that CTL vs. NCTL had no effects on PENASP. This could be attributed to floor effects (not so many subjects aspirated on NCTL to exhibit important differences in response to CTL) as only 3 of 14 participants in the study sample aspirated on NCTL. It was hypothesized that the participants would have faster initiation of the pharyngeal swallow when drinking CTL than when drinking NCTL. This faster initiation would be reflected in shorter STD and lower IPS ratings and consequently in a more proximal bolus position at the swallowing initiation. However, CTL had no significant effect on the IPS scores of 5-, 10-, and 25-ml swallows. This is partially in accordance with the STD findings as no significant differences were found on the STD of 5- and 10-ml swallows as well. In both outcome measures the effect sizes indicated a slightly faster pharyngeal response on 5 and 10 ml with CTL vs. NCTL. Floor effect again might be a possible explanation for the insignificant findings in this study. The normative mean STD for 5 and 10 ml of liquid in an age-matched healthy group is -0.03 (abnormal C0.49) and 0.00 (abnormal

K. Sdravou et al.: Effects of Carbonated Liquids

C0.52), respectively [43]. Therefore, what is seen radiographically as a delay in the pharyngeal response can be judged as normal for people without dysphagia. In this study, 11 of the 17 participants (65%) had normal (\0.49) STD on 5 ml NCTL and 7 of 12 (58%) had normal (\0.52) STD on 10 ml NCTL. This explanation is in accordance with Krival [26] who also reported that her sample did not have a sufficiently lengthy STD on 5 ml NCTL to be able to reflect change on 5 ml CTL. Of interest, a statistically significant increase in STD was found in response to CTL on 25 ml (P = 0.031). In a previous study comparing chemesthetic stimuli to thin liquids only, Pelletier and Lawless [22] examined continuous cup drinking. In contrast to the present study, they did not find significant effects of the sour bolus on STD, mainly because only one subject had abnormal STD. This study and the Pelletier and Lawless study also have some important differences in methodology, including the instrumental assessment used (VFSS vs. FEES) and consequently the operational definitions of STD, which make comparison of findings challenging. However, the statistically large increase in STD of the 25-ml swallow was not reflected in the IPS scores in this study. One possible explanation for this difference is that less overt responses to bolus characteristics can be best identified by temporal measures such as STD. Hence, it seems that although CTL have a significantly increased STD on 25 ml, this is not of real clinical significance. CTL did not significantly reduce the temporal measures of OTT and PTT for any volume of bolus. This result was not expected and it differs from that of studies that have reported reduced temporal measures in response to chemesthetic stimuli such as sour and carbonated liquids [21, 24, 29]. One possible explanation for this disparity is that the participants in this study were not screened a priori to determine whether they had oral phase dysphagia or prolonged enough PTT on NCTL to exhibit reductions in response to CTL. Another possible explanation for this finding might be the heterogeneity of the participants relative to the neurological etiology. Logemann et al. [21] found significantly shorter OTT on sour (chemesthetic) thin liquids vs. nonsour thin liquids only for the stroke group, whereas no difference was found for the group with other neurological etiologies. In the present study, citric acid was also an element of the carbonated stimulus and people with TBI were also included. Perhaps chemesthetic stimuli might have significant effects on OTT in people with stroke but not in people suffering from other neurological conditions. The methodological differences of measuring OTT could be another factor that might lead to inconclusive findings. In the Logemann et al. study [21] the participants were asked to execute cued swallows. As a result, OTT was dependent on the bolus movement following the command.

However, in the present study the participants were asked to execute spontaneous, noncued swallows. Consequently, the OTT in this study was exclusively dependent on tongue movement. It was hypothesized that retention would have been reduced significantly in response to CTL. However, CTL vs. NCTL had no significant effects on PR of 5-, 10-, and 25-ml swallows. These findings are in keeping with those of Krival [26] who used the same scale of PR as the present study. Bulow et al. [24] and Nixon [29], who both reported significantly less retention with CTL, have used different scales of PR. As there is no single accepted rating of pharyngeal retention and there is great variability among judges in rating PR, the validity and reliability of PR scales are questionable. The present study, however, has provided strong inter- and intrarater reliability indicators of the PR findings which strengthen their reliability. Again, the most plausible explanation for the unanticipated outcome might be the floor effect as about 50% of the participants did not have any pharyngeal residue after NCTL. A further consideration is the age of the participants in this study; they were heterogeneous in terms of age. It is known that aging results in a reduction in sensory receptors and that both motor and sensory nerve fibers exhibit slowed conduction velocities [44]. Different age groups may show different responses to sensory input and this must be examined in further research. The group was also heterogeneous with respect to time post onset of dysphagia. Patient compliance and the acceptability of compensatory measures is a key issue for SLPs, and while other chemesthetic stimuli such as sour liquids also have been found to reduce the risk of bolus penetration [21], palatability limits their use in clinical practice. Consequently, if a palatable stimulus could reduce the risk of aspiration, its potential benefit could be significant for people with dysphagia. Sensation elicited by carbonated beverages is pleasurable for many people despite the fact that it can be irritating or even painful to some people [45] and, participants in this study had a marked tendency (p = 0.052) to like CTL.

Conclusion While challenged by the availability of robust valid and reliable outcome measures, we conclude that CTL shows promise in significantly reducing penetration and aspiration in people with CNS neurogenic dysphagia. It is theorized that chemesthetic stimuli such as carbonation excite peripheral sensory receptors and activate sensory fibers in the NTS of the brainstem, which is the main structure responsible for swallow initiation [16, 17, 19, 45–51]. Although in the present study CTL did not elicit a faster

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K. Sdravou et al.: Effects of Carbonated Liquids

swallowing response, it did significantly decrease penetration and aspiration compared to NCTL. The mucosa of the pharynx and larynx is supplied with mechanoreceptors, chemoreceptors, nociceptors, and thermoreceptors, which all are purported to respond to chemesthetic stimuli. Stimulation of these receptors gives rise to protective reflexes which serve to prevent aspiration of bolus into the airway [52]. It seems that the chemesthetic properties of the CTL did provide a strong stimulation to the highly reflexogenic area of the larynx, resulting in reduced aspiration and consequently in better protection of the upper airway. There are some limitations to this study that must be considered when designing further research in the area. Statistical power analysis suggested a sample size of 27 people but only 17 met the inclusion criteria, lowering the power of the results (a level of 0.05) to 0.62. Financial and clinical resources did not permit an extension on the project to collect additional data. Larger population samples to examine the effects of CTL on swallow function and parameters other than penetration/aspiration are needed to avoid the floor effect, as described here. In addition, the categorization of participants a priori to include people with abnormal OTT, PTT, PENASP, and PR is recommended. It remains unknown whether commercial carbonated beverages would have similar effects on swallowing physiology. Thus, each person with dysphagia must be individually evaluated to assure that CTL will affect his/her swallowing performance positively for the additional reason that aspiration consequences of such an acidic material would be more challenging. CTL may be ill advised for individuals with reflux because the buildup of gases distends the stomach and may pressurize the UES. Overall, we conclude that CTL should be a beneficial and palatable treatment option for people with aspiration on NCTL but much more research is required. For example, its efficacy should be examined in more specific homogeneous populations such as those with stroke. This would allow for subgroup analyses (i.e., lesion site, time post onset, age) that might unearth some important insights into the efficacy of CTL when mapped with specific neurological impairments. To further expose the clinical significance of CTL, future research should establish whether CTL has an impact on patient hydration levels and, most importantly, on quality of life. This study serves to extend the debate in this area of clinical dysphagia research. Acknowledgments The authors thank the 17 people who participated in this study, the speech-language pathologist who provided reliability data, and Dr. Nikolao Tsigili, Aristotle University, who aided in the statistical analysis of the data.

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MSc

Margaret Walshe

MSc, PhD

Lukas Dagdilelis

MD

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