Dysphagia DOI 10.1007/s00455-014-9538-5
ORIGINAL ARTICLE
Tongue Pressure During Swallowing in Adults with Down Syndrome and Its Relationship with Palatal Morphology Megumi Hashimoto • Kazuko Igari • Soshi Hanawa Ayumi Ito • Atsushi Takahashi • Naoko Ishida • Shigeto Koyama • Takahiro Ono • Keiichi Sasaki
•
Received: 11 November 2013 / Accepted: 18 April 2014 Ó Springer Science+Business Media New York 2014
Abstract In individuals with Down syndrome, hypotonicity of the tongue and an underdeveloped maxilla may lead to poor oral motor coordination, which adversely affects the oral phase of swallowing. This study aimed to evaluate the characteristics of pressure produced by the tongue against the hard palate during swallowing in individuals with Down syndrome. In addition, the relationship between tongue pressure and palatal morphology was examined. We studied nine adults with Down syndrome and ten healthy adults as controls. Tongue pressure while swallowing 5 mL water was recorded by a sensor sheet system with five measuring points attached to the hard palate. Palatal length, depth, width, curvature, and slope were measured by three-dimensional digital maxillary imaging. The order of onset of tongue pressure on the median line of the hard palate was the same in all participants, except for three with Down syndrome. The duration and maximal magnitude of tongue pressure on the median
line in nine participants with Down syndrome were significantly shorter and lower than those of controls. In participants with Down syndrome, significant positive correlations were observed between the duration of tongue pressure at the mid-median part of the hard palate and palatal depth and width, and between the duration and maximal magnitude of tongue pressure at the posteriormedian part and palatal length. These findings suggest that impaired tongue activity, poor tongue control, and constrained tongue motion due to a short and narrow palate contribute to swallowing difficulty in individuals with Down syndrome. Keywords Down syndrome Swallowing Tongue pressure Palatal morphology Deglutition Deglutition disorders
Introduction M. Hashimoto (&) S. Hanawa N. Ishida K. Sasaki Division of Advanced Prosthetic Dentistry, Tohoku University Graduate School of Dentistry, 4-1 Seiryo-machi, Aoba-ku, Sendai 980-8575, Japan e-mail: [email protected] M. Hashimoto K. Igari A. Ito A. Takahashi N. Ishida K. Sasaki Clinics of Dentistry for the Disabled, Tohoku University Hospital, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan S. Koyama Maxillofacial Prosthetics Clinic, Tohoku University Hospital, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan T. Ono Department of Prosthodontics, Gerodontology and Oral Rehabilitation, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka 565-0871, Japan
Down syndrome (DS), the most common chromosomal disorder, is characterized by developmental disabilities. Many individuals with DS have functional problems associated with mastication and swallowing [1–8], which are caused by neuromotor dysfunction, orofacial dysmorphology, dental abnormalities, and developmental delay [4, 9]. Underdevelopment of the maxilla, together with a narrow and short palate, has previously been described [10–12]. In addition, hypotonicity of the orofacial muscles, especially the tongue, is also common in DS [13, 14]. Consequently, individuals with DS have a hypotonic tongue in a relatively small oral cavity. These anatomical and neuromotor abnormalities may lead to poor oral motor coordination, such as open-mouth posture, tongue protrusion, and lack of stability of the mandible during mastication and swallowing
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[5, 9]. The tongue makes an important contribution to bolus transit during swallowing: contact pressure between the anterior tongue and the palate facilitates the beginning of the oral transport phase of swallowing [15], after which the tongue elevates a bolus to the palate, rolling and propelling it toward the pharynx by applying sequential anterior–posterior pressure [16]. Tongue pressure produced by contact between the hard palate and tongue is a major propulsive force in the transport of a food bolus toward the pharynx [17]. Inadequate generation of tongue pressure may indicate impaired tongue activity during swallowing. Stierwalt and Youmans [18] reported that reduced maximal isometric contraction of the tongue was evident in patients with oral dysphagia. Konaka et al. [19] have shown that the maximal magnitude of tongue pressure during swallowing in patients with dysphagia after stroke was lower than in those without dysphagia. They also reported that patients with dysphagia had a polyphasic pattern of tongue pressure, which suggested repetitive tongue movement as compensation for lower tongue pressure. Gisel et al. [1] reported that most 4- and 5-year-old children with DS protrude the tongue during swallowing, and they did not make the transition from infantile swallowing to the mature type of swallowing seen in agematched typically developing children. Smith et al. [20] reported that inadequate lip closure, impaired tongue movement, and lack of stability of the mandible were often observed during swallowing in adults with DS, although in their study the majority of participants were either edentulous or had very few teeth. The impairment of oral motor coordination, inadequate lip closure, and weak and impaired tongue movement make it difficult to acquire the basic functions of mastication and swallowing [8]. Difficulty in keeping food in the mouth [20], longer mastication time [2], reduced chewing frequency [7], and difficulty transferring a bolus [3] during eating and drinking have been observed in individuals with DS. Several studies have noted that anatomical abnormality of the oral cavity affected the oral phase of swallowing in individuals with DS [5, 9, 20, 21]. However, it is not clear how maxillary hypoplasia with a short and narrow palate influences tongue function during swallowing in individuals with DS. In more than half of children with DS, delayed initiation of the swallowing response and liquid aspiration were found in studies of swallowing function using videofluoroscopy [3, 22]. One report found that coughing during eating and drinking was observed in one half of adults with DS [20], which is suggestive of aspiration. As a result of swallowing difficulties lasting into adulthood, general health can be affected by respiratory illness or poor nutrition. Some therapies improve oral motor function, and this is considered to have a positive effect on development of mastication and swallowing in individuals with DS.
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Longitudinal observational studies have shown that early stimulating-plate therapy in physiotherapeutic practice in children with DS improves mouth posture and tongue position at rest [23, 24]. Subjective observational assessment of orofacial appearance has been widely used to evaluate mouth posture and tongue position in individuals with DS; however, this method cannot establish muscle strength and tongue function in a closed mouth. A more detailed, objective technique is needed to assess tongue function during swallowing. Electropalatography is a useful means of evaluating the temporal change of tongue contact position on the palate, but it does not measure contact pressure between the tongue and palate. Several studies that examine tongue pressure using pressure sensors have been conducted [16, 17, 25– 27]. Ono et al. [16] measured tongue pressure in healthy young adults using an experimental palatal plate that contained seven pressure sensors. They determined the normal pattern of tongue pressure production during swallowing by analyzing the time of onset, peak, and offset; duration; and maximal magnitude of tongue pressure. Based on this study, Hori et al. [28] developed a tactile sensor sheet with five measuring points that allows the measurement of tongue pressure during swallowing. The sensor sheet is sufficiently thin so that tongue pressure can be measured with little discomfort after a short familiarization period. This sensor sheet has been used to study not only elderly healthy volunteers but also patients after stroke [19, 29–31]. Therefore, we felt that the sensor sheet could be used to measure tongue pressure generation in individuals with DS who might have a limited ability to cooperate. We aimed to determine the characteristics of tongue pressure during swallowing in individuals with DS using the sensor sheet, and to compare timing of onset, peak, and offset; duration; maximal magnitude; and the integrated value of tongue pressure with those recorded in healthy individuals. In addition, we aimed to determine the effect of the characteristic palatal morphology of DS on tongue pressure. We hypothesized that duration, maximal magnitude, and integrated value of tongue pressure in adults with DS would be shorter and lower compared with those of healthy adult volunteers, and that the specific morphological changes to the palate in adults with DS would influence tongue pressure during swallowing.
Methods Participants The study population consisted of nine adults with DS. All were men with a mean (±standard deviation [SD]) age of 26.0 ± 5.9 years (range = 20–35 years) who were managed
M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome
regularly at the dental clinics of Tohoku University Hospital, Japan. Ten healthy volunteers matched for sex and age within 5 years of the participants were enrolled as controls (mean age = 26.0 ± 1.8 years; range = 24–30 years). Criteria for exclusion of participants with DS were a clinical history of prosthodontic treatment and loss of more than three teeth on either side. We also excluded potential participants with evidence of loss of occlusal support, namely, instability of the mandible, because of failure to achieve posterior occlusal contact, which could influence our measurements by impairing the normal mechanism of transporting a food bolus from the oral cavity to the pharynx [32]. All participants with DS had more than 24 natural teeth and consumed a normal diet. Criteria for exclusion of controls were a clinical history of deglutition disorder, orthodontic treatment, or temporomandibular disorder, any tooth loss except for the third molars, and occlusion abnormality. Written informed consent was obtained from the parents of participants with DS and from the controls. Oral agreement was obtained from each participant with DS with the capacity to do so. Conduct of the study was approved by the Ethics Committee of Tohoku University Graduate School of Dentistry (Nos. 22–28).
Fig. 1 Palatal view of the maxilla after attaching the sensor sheet in a participant with Down syndrome
Measurement of Tongue Pressure A tactile sensor system with a 0.1-mm-thick sensor sheet (Swallow scan; Nitta, Osaka, Japan) was used for the measurement of tongue pressure. The sensor sheet contains five measurement points (channels [Chs.] 1–5). According to the technique described by Hori et al. [28], three measurement points, Chs. 1–3, were placed along the median line of the palate. Ch. 1 was placed at the anterior-median part, Ch. 2 at the mid-median part, and Ch. 3 at the posterior-median part of the palate. The other two measurement points, Chs. 4 and 5, were placed at the right and left posterior-lateral part of the hard palate, respectively (Fig. 1). One sensor sheet was used for each participant; one of three sizes was selected to fit the palate. The sheet was directly attached to the palate with a sheet-type denture adhesive (Touch Correct II; Shionogi, Osaka, Japan), and a recording wire leading to a computer was passed through the oral vestibule without hindrance to occlusion. Before measurements were taken, the system was calibrated by applying negative pressure of a known value onto the sensor sheet using a vacuum pump attached to an air duct within the recording wire, mimicking positive pressure applied uniformly to each sensor. While taking measurements, the participant was seated in an upright position with feet on the floor. Each participant was asked to take 5 mL water (at 37 °C) into the mouth from a syringe and swallow when instructed. Five recordings of tongue pressure were made for each participant at intervals
Fig. 2 a Representative output signals of tongue pressure while 5 mL water is swallowed by a healthy participant. b Typical output of measurement of tongue pressure in Ch. 1
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of more than 1 min. The output signals of tongue pressure at Chs. 1–5 for each swallow were also recorded (Fig. 2a). The time of onset, peak, and offset; duration; maximal magnitude; and integrated value of tongue pressure for each waveform of Chs. 1–5 were analyzed later (Fig. 2b). Analyses of Palatal Morphology Alginate impressions of the participants’ maxillae were taken and a hard plaster cast was made. The following landmarks were marked on each cast: the incisive papilla (IP), the right and left hamular notches (HR, HL), and the deepest points of the gingival margin in the apical direction at the upper first molars on the right and left sides (MR, ML). A three-dimensional (3D) digital maxillary image was created from the cast on a personal computer by using a noncontact 3D digitizer with a resolution of 248 points/mm2 (NextEngine HD Pro; NextEngine, Inc., Santa Monica, CA, USA) and software (RapidWorks; Rapidform Japan, Tokyo, Japan). The 3D images of the maxilla and the landmarks on the cast were used to determine standardized measurements of the horizontal plane defined by IP, HR, and HL, and of the coronal plane, defined as the plane containing the line MR– ML perpendicular to the horizontal plane. The intersection point of the median palatine suture and the coronal plane (M) and the foot of the perpendicular line from M to the line MR–ML (MM) were also determined. Furthermore, 32 points that included MR, M, and ML were placed on the cross-sectional line of the palatal surface and the coronal plane to determine palatal curvature in the coronal section, with 15 points projected vertically from the points dividing the line segment MR–ML at regular intervals. In addition, 14 points were projected horizontally onto the right and left sides of the palate from the seven points dividing the line MM–M into eight equal portions. Thus, the following parameters were calculated for each participant: (1) palatal length: the distance between IP and the line HR–HL (Fig. 3a); (2) palatal depth: the distance between MM and M (Fig. 3b); (3) palatal width: the distance between MR and ML (Fig. 3b); and (4) palatal curvature (a): the curvature of the palate in the coronal section, defined as follows [33–35]. The curved line formed by 32 points on the palatal surface between MR and ML was approximated to a parabola: y = ax2 ? b. Perrier et al. [36] previously reported that a is described by the coefficient a from the equation for the parabola as 4 a ¼ pffiffiffiffiffiffi 3 j aj A high a value indicates a flat palate and a low a value indicates a sharp curved palate in the coronal section. The fifth parameter was palatal slope, defined as the angle made by the line IP–M with the horizontal plane (Fig. 3c).
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Fig. 3 Landmarks of palatal morphology in a three-dimensional (3D) digital image from the maxillary dental cast of a participant with Down syndrome (DS). a Palatal view. b Coronal view. c Sagittal view. IP, incisive papilla; HR, right hamular notch; HL, left hamular notch; MR, the deepest point of the gingival margin to the apical direction at the right first molar; ML, the deepest point of the gingival margin to the apical direction at the left first molar; M, intersection point of the median palatine suture and the coronal plane, defined as the plane containing the line MR–ML, perpendicular to the horizontal plane; MM, base of the perpendicular line from M to the line MR– ML. The horizontal plane is defined by IP, HR, and HL. Parameters of palatal morphology: (A), palatal length; (B), palatal depth; (C), palatal width; and (D), palatal slope
Statistical Analyses Differences in the timing of onset, peak, and offset of tongue pressure at five measurement points (Chs. 1–5) were compared using Friedman’s test, followed by the Wilcoxon signed-ranks test with Bonferroni’s correction as a post hoc analysis to test the differences between Chs. To examine whether there were differences in duration and maximal magnitude of tongue pressure among the five swallows in each of the five Chs., one-way repeated-measures analysis of variance (ANOVA) was performed for each group. The interaction and main effects in the
M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome
duration, maximal magnitude, and integrated value of tongue pressure in the five Chs. for the participants with DS and the controls were examined using two-way repeatedmeasures ANOVA, with the group as the independent variable and the measurement point as the dependent variable. In case of violation of assumption of sphericity, the degree of freedom was corrected using the Huynh-Feldt e. Significant interactions were analyzed by the simple maineffects test. We conducted Bonferroni’s test and the Welch test as post hoc analyses of the two-way repeated ANOVAs for Chs. and groups, respectively. Differences between the five parameters of palatal morphology were analyzed using the Mann–Whitney U test. Correlations between the duration and maximal magnitude of tongue pressure and the five parameters of palatal morphology were evaluated using Spearman’s correlation coefficients. Statistical significance was accepted as p \ 0.05. Data were analyzed using IBM SPSS ver. 21.0 (IBM Japan, Tokyo, Japan).
measurement point (F [3.40, 57.81] = 2.93, p = 0.035). The main effects between groups (F [1, 17] = 11.22, p = 0.004) and between measurement points (F [3.40, 57.81] = 19.75, p \ 0.001) were also significant. The duration of tongue pressure in participants with DS was significantly shorter than in controls at Chs. 1, 2, and 3 (p \ 0.01, Fig. 4a). Within the DS group, the duration of tongue pressure was significantly shorter at Chs. 1 and 2 (p \ 0.05) and Ch. 3 (p \ 0.01) than at Ch. 5. Within controls, the duration of tongue pressure at Ch. 1 was significantly longer than at Ch. 3 (p \ 0.05). In both groups, the duration of tongue pressure at Ch. 3 was significantly shorter than that at Chs. 4 and 5 (participants with DS, p \ 0.01; controls, p \ 0.05; Fig. 4a). Tongue pressure was significantly shorter on the median line of the palate (Chs. 1–3), especially in Ch. 1, in the participants with DS. Maximal Magnitude of Tongue Pressure
Three out the nine participants with DS showed partial pressure or no tongue pressure in Chs. 1–3. In the remaining six participants with DS, the order of onset of tongue pressure in Chs. 1–3 was from Ch. 1 to Ch. 2 and then Ch. 3. This sequential pattern of tongue pressure onset was the same as that in all controls. No significant difference was found in the timing of the onset, peak, and offset of tongue pressure in Chs. 1–5 between these six participants with DS and the controls.
A significant main effect was found for the maximal magnitude of tongue pressure between groups (F [1, 17] = 15.74, p = 0.001) and between measurement points (F [1.75, 29.71] = 9.76, p = 0.001). There was no significant relationship between group and measurement point (F [1.75, 29.71] = 1.36, p = 0.27). The maximal magnitude of tongue pressure in participants with DS was significantly lower than in controls at all measuring points, except for Ch. 4 (Chs. 1–3, p \ 0.01; Ch. 5, p \ 0.05; Fig. 4b). In participants with DS, the maximal magnitude of tongue pressure at Ch. 3 was significantly lower than at Ch. 4 (p \ 0.05) and at Ch. 5 (p \ 0.01). Within controls, the maximal magnitude of tongue pressure at Ch. 2 was significantly greater than at Ch. 3 (p \ 0.05; Fig. 4b). Overall, the maximal magnitude of tongue pressure on the palate was lower in participants with DS than in controls.
Inter- and Intra-individual Variability of Duration and Maximal Magnitude of Tongue Pressure
Integrated Values of Tongue Pressure
Results Order of Onset of Tongue Pressure
The pattern of tongue pressure in participants with DS varied considerably between individuals compared with controls. The duration and maximal magnitude of tongue pressure in participants with DS showed a trend toward shorter and lower values in Chs. 1–3 than those of controls. Analysis of intra-individual variability of the duration and maximal magnitude of tongue pressure found no significant difference among the five swallows at all five channels in both groups (participants with DS, p [ 0.05; controls, p [ 0.05). Duration of Tongue Pressure Analysis of the duration of tongue pressure showed a statistically significant relationship between group and
Analysis of the integrated value of tongue pressure showed a significant relationship between group and measurement point (F [3.05, 51.78] = 3.10, p = 0.034). The main effects between groups (F [1, 17] = 21.81, p \ 0.001) and between measurement points (F [3.05, 51.78] = 12.62, p \ 0.001) were also significant. The integrated values of tongue pressure in participants with DS were significantly lower than those in controls at all measurement points, except for Ch. 3 (p \ 0.01; Fig. 4c). In participants with DS, the integrated value at Ch. 3 was significantly lower than at Ch. 5 (p \ 0.05). Within controls, the integrated values at Chs. 1, 4, and 5 were significantly higher than those at Ch. 3 (p \ 0.01; Fig. 4c). In general, the integrated value of tongue
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M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome Fig. 4 Comparisons of the (a) duration, (b) maximal magnitude, and (c) integrated value of tongue pressure at each measurement point (Chs. 1–5) during swallowing in participants with DS and controls
pressure on the palate was lower in participants with DS, especially in Ch. 1. Correlations Between Duration and Maximal Magnitude of Tongue Pressure and Palatal Morphology The results of analyses of palatal morphology are shown in Table 1. Palatal length, width, and curvature in participants with DS were significantly lower than those in controls (palatal length, p \ 0.001; palatal width and curvature, p \ 0.01). There was no significant difference in palatal depth or slope between the groups.
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The duration of tongue pressure at Ch. 2 was significantly positively correlated with the palatal depth and width, and that at Ch. 3 was significantly positively correlated with palatal length in participants with DS (Table 2). In controls, there was no significant correlation between the duration of tongue pressure and palatal morphology. The maximal magnitude of tongue pressure at Ch. 3 was significantly positively correlated with palatal length, and at Ch. 5 it was significantly negatively correlated with palatal width in participants with DS (Table 3). In controls, the maximal magnitude of tongue pressure at Ch. 3 was significantly positively correlated with palatal width and curvature.
M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome Table 1 Palatal length, depth, width, curvature (a), and slope in participants with Down syndrome (DS) and controls Participants with DS (n = 9) Parameters
Median (IQR)
Controls (n = 10) Range
Median (IQR)
Range
p
Palatal length (mm)
39.11 (37.93–41.18)
36.38–42.36
45.80 (45.24–48.29)
42.47–49.77
\0.001
Palatal depth (mm)
12.79 (12.11–13.75)
11.91–14.60
12.74 (11.76–13.51)
8.46–15.07
0.568
Palatal width (mm)
29.72 (26.64–32.19)
22.47–41.44
35.94 (33.66–38.21)
31.06–43.16
0.007
Palatal curvature (a) Palatal slope (°)
1.69 (1.47–1.76)
1.31–2.23
2.00 (1.88–2.15)
1.81–2.73
0.003
29.40 (26.58–31.89)
21.64–36.14
27.77 (26.56–28.88)
16.10–31.55
0.191
Table 2 Spearman’s correlation coefficients (r) between the duration of tongue pressure and five parameters of palatal morphology in participants with Down syndrome (DS) and controls Group
Channel
Participants with DS (n = 9)
Ch. 1
0.43
0.52
0.52
0.47
Ch. 2
0.27
0.68*
0.78*
0.61
-0.17
Ch. 3
0.71*
-0.13
0.34
0.50
-0.55
Ch. 4
0.50
0.48
0.18
0.15
0.03
Controls (n = 10)
Palatal length
Palatal depth
Palatal width
Palatal curvature (a)
Palatal slope -0.05
Ch. 5
0.37
0.53
0.18
0.08
0.18
Ch. 1
-0.48
-0.12
-0.21
-0.09
0.39
Ch. 2 Ch. 3
0.10 0.25
-0.12 0.14
0.19 0.60
0.24 0.55
0.39 0.29
Ch. 4
0.08
0.06
-0.43
-0.26
-0.02
Ch. 5
0.53
-0.42
0.20
0.42
-0.47
* p \ 0.05
Table 3 Spearman’s correlation coefficients (r) between the maximal magnitude of tongue pressure and five parameters of palatal morphology in participants with Down syndrome (DS) and controls Group
Channel
Participants with DS (n = 9)
Ch. 1
0.22
0.27
0.20
0.35
Ch. 2
0.15
0.61
0.39
0.41
-0.17
Ch. 3
0.73*
-0.13
0.10
0.32
-0.65
Ch. 4
0.65
-0.03
-0.30
-0.08
-0.23
Ch. 5
0.50
-0.20
-0.73*
-0.48
-0.07
Ch. 1
0.16
-0.24
0.36
0.29
-0.32
Ch. 2 Ch. 3
0.19 -0.16
-0.26 -0.15
0.49 0.72*
0.49 0.67*
-0.16 -0.10
Controls (n = 10)
Palatal length
Palatal depth
Palatal width
Palatal curvature (a)
Palatal slope -0.22
Ch. 4
0.02
0.18
-0.03
-0.15
0.12
Ch. 5
-0.26
-0.04
0.15
0.13
-0.06
* p \ 0.05
Discussion This is the first study that examined the generation of tongue pressure in individuals with DS as a measure of tongue function during swallowing. Characteristic differences in the duration, maximal magnitude, and integrated value of tongue pressure between participants with DS and controls were found. In addition, tongue pressure was
correlated with the palatal length, depth, and width in participants with DS. We found partial tongue pressure or no tongue pressure at the measurement points on the median line in three of nine participants with DS. Therefore, we compared the order of onset of tongue pressure in the remaining six participants with DS with that recorded in the ten controls. Consistent with the study of Ono et al. [16], tongue
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pressure on the median line was generated from the anterior-median part to the mid-median part of the palate, and then to the posterior-median part in controls. This sequential pattern in the onset of tongue pressure in controls was the same as the six participants with DS. This finding, and the considerable interindividual differences observed, suggests that tongue function during swallowing varies widely in individuals with DS. Hypotonicity of the tongue could be one factor that causes shorter duration, lower maximal magnitude, and integrated value of tongue pressure in participants with DS. A decline in the duration and maximal magnitude of tongue pressure from anterior to posterior on the median line of the hard palate is a normal pattern of tongue pressure production in healthy individuals [16]. In controls, the duration and maximal magnitude of tongue pressure was essentially normal; however, there was no significant difference in the duration and maximal magnitude between the measurement points on the median line in participants with DS. Differences between participants with DS and controls could be explained by neuromotor dysfunction, abnormal palatal morphology, and maxillofacial structure, or both. Hamilton [37] proposed that tongue protrusion beyond the anterior teeth during articulation of alveolar sounds in adults with DS could result from difficulty in motor control of the tongue tip. Participants with DS in this study could swallow water with the mouth closed; however, the lower maximal magnitude and the shorter duration of tongue pressure at the anterior-median part of the palate (Ch. 1) in participants with DS indicated that the tongue tip might be positioned in a lower and more anterior position to the IP because of poor ability to control the tip. We also found that the length and width of the palate in participants with DS were significantly shorter than those in controls, but there was no significant difference in the depth of the palate between groups. These findings are in agreement with a study by Shapiro et al. [10]. The median value of the palatal curvature in the controls was 2.00 in our study, broadly comparable with the mean value of palatal curvature (1.93) in 11 healthy young men reported by Yunusova et al. [34]. The significantly lower value of the palatal curvature (median: 1.69) in participants with DS than in controls indicates that participants with DS had a steep curved palate in the coronal section. Some investigators have suggested that tongue movement during swallowing is related to maxillofacial morphology [38–40]. Go¨rgu¨lu¨ et al. [40] reported that the tongue tip was more anterior and the posterior border of contact between the tongue and the palate was more anterior during swallowing in individuals with class III malocclusion and maxillary retrognathism than in those with class I malocclusion. We found significant positive correlations between
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the duration and maximal magnitude of tongue pressure and the palatal length at the posterior-median part of the palate (Ch. 3). Although the position of the mandible related to the maxilla was unknown, these results suggest that a shorter palatal length was a factor in positioning the tongue anterior to the maxilla, which affected tongue pressure generation against the posterior-median part of the palate. Contact of the tongue tip with the lingual surface of the anterior teeth could be a way to seal the anterior oral cavity to adapt to an underdeveloped maxilla with a shorter palatal length in individuals with DS. Furthermore, we found significant positive correlations between the duration of tongue pressure and the palatal depth and width at the mid-median part of the palate (Ch. 2). Cheng et al. [39] reported that palatal depth and dental arch length, but not palatal width, were positively correlated with the magnitude of tongue movement during swallowing in healthy young adults. Unlike in healthy adults, a narrower palatal width is suspected to be the cause of constraint on tongue motion in participants with DS. In one participant with DS, who had the least palatal curvature (1.31), the narrowest width (22.47 mm), and the third shortest palatal length (37.79 mm) of all participants with DS, there was no tongue pressure on the median line (Chs. 1–3). Generally, the palatal morphology of individuals with DS deviates from normal more than that of healthy individuals. In addition, individuals with DS may have less capacity to adapt to abnormal palatal morphology than healthy individuals because of neuromotor dysfunction. Our study showed a significant correlation between tongue pressure during swallowing and palatal morphology in participants with DS; however, whether impaired tongue pressure causes palatal hypoplasia or whether abnormal palatal morphology constrains tongue movement is unclear. Further research is required to establish whether functional training of the tongue can promote normal growth of the palate, and how tongue pressure can change if orthodontic treatment is provided to expand the palate in individuals with DS. Our study had several limitations. First, the small sample size, the result of difficulty in recruiting participants with DS, limited the statistical power. Second, biased sampling, because of difficulty applying the experimental protocol to the entire population with DS, limits the generalizability of our findings. Depending on the extent of intellectual disability, individuals with DS appeared to find it difficult to tolerate the sensor sheet against their palate and to swallow when directed. Nonetheless, the technique could be used in most of the adults with DS who regularly visit our hospital for dental treatment or surveillance. Third, the sensor sheet did not fit the small palate of women with DS; a smaller sheet is required for use in children or women with DS.
M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome
Although we investigated the relationship between tongue pressure and palatal morphology in participants with DS, tongue function during swallowing is affected by numerous factors such as the position of the mandible related to the maxilla, its stability, the size of the tonsils, and breathing through the mouth. Further studies are required to understand tongue function during swallowing and how it may be different in individuals with DS. To encourage development of oral motor skills associated with mastication and swallowing in individuals with DS, appropriate support—tailored to an individual’s level of understanding, capability, and compliance—is required. Evaluation of tongue function and palatal morphology can provide important information on the choice of proper food or to guide intervention. Therefore, tongue pressure measurements could be a useful guide for evaluating the therapeutic effects of interventions designed to improve tongue function in individuals with DS. In conclusion, impaired tongue activity, poor tongue control, and constrained tongue motion due to a short and narrow palate are likely to contribute to swallowing difficulties in individuals with DS. Acknowledgments We thank Dr. Nobue Goto, Dr. Hitomi Ando, and the staff at the Clinics of Dentistry for the Disabled, Tohoku University Hospital. We also thank all the participants in this study. Conflict of interest declare.
The authors have no conflicts of interest to
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10. Shapiro BL, Gorlin RJ, Redman RS, Bruhl HH. The palate and Down’s syndrome. N Engl J Med. 1967;276:1460–3. 11. Fink GB, Madaus WK, Walker GF. A quantitative study of the face in Down’s syndrome. Am J Orthod. 1975;67:540–53. 12. Alio J, Lorenzo J, Iglesias MC, Manso FJ, Ramirez EM. Longitudinal maxillary growth in Down syndrome patients. Angle Orthod. 2011;81:253–9. 13. Yarom R, Sherman Y, Sagher U, Peled IJ, Wexler MR, Gorodetsky R. Elevated concentrations of elements and abnormalities of neuromuscular junctions in tongue muscles of Down’s syndrome. J Neurol Sci. 1987;79:315–26. 14. Hoyer H, Limbrock GJ. Orofacial regulation therapy in children with Down syndrome, using the methods and appliances of Castillo-Morales. ASDC J Dent Child. 1990;57:442–4. 15. Schindler JS, Kelly JH. Swallowing disorders in the elderly. Laryngoscope. 2002;112:589–602. 16. Ono T, Hori K, Nokubi T. Pattern of tongue pressure on hard palate during swallowing. Dysphagia. 2004;19:259–64. 17. Shaker R, Cook IJ, Dodds WJ, Hogan WJ. Pressure-flow dynamics of the oral phase of swallowing. Dysphagia. 1988;3:79–84. 18. Stierwalt JA, Youmans SR. Tongue measures in individuals with normal and impaired swallowing. Am J Speech Lang Pathol. 2007;16:148–56. 19. Konaka K, Kondo J, Hirota N, Tamine K, Hori K, Ono T, Maeda Y, Sakoda S, Naritomi H. Relationship between tongue pressure and dysphagia in stroke patients. Eur Neurol. 2010;64:101–7. 20. Smith CH, Teo Y, Simpson S. An observational study of adults with Down syndrome eating independently. Dysphagia. 2013;29:52–60. 21. Lazenby T. The impact of aging on eating, drinking, and swallowing function in people with Down’s syndrome. Dysphagia. 2008;23:88–97. 22. O’Neill AC, Richter GT. Pharyngeal dysphagia in children with Down syndrome. Otolaryngol Head Neck Surg. 2013;149:146–50. 23. Hohoff A, Ehmer U. Short-term and long-term results after early treatment with the Castillo Morales stimulating plate. A longitudinal study. J Orofac Orthop. 1999;60:2–12. 24. Korbmacher HM, Limbrock JG, Kahl-Nieke B. Long-term evaluation of orofacial function in children with Down syndrome after treatment with a stimulating plate according to Castillo Morales. J Clin Pediatr Dent. 2006;30:325–8. 25. Chiba Y, Motoyoshi M, Namura S. Tongue pressure on loop of transpalatal arch during deglutition. Am J Orthod Dentofacial Orthop. 2003;123:29–34. 26. Kieser J, Singh B, Swain M, Ichim I, Waddell JN, Kennedy D, Foster K, Livingstone V. Measuring intraoral pressure: adaptation of a dental appliance allows measurement during function. Dysphagia. 2008;23:237–43. 27. Steele CM, Van Lieshout PH. The dynamics of lingual-mandibular coordination during liquid swallowing. Dysphagia. 2008;23:33–46. 28. Hori K, Ono T, Tamine K, Kondo J, Hamanaka S, Maeda Y, Dong J, Hatsuda M. Newly developed sensor sheet for measuring tongue pressure during swallowing. J Prosthodont Res. 2009;53:28–32. 29. Hori K, Ono T, Iwata H, Nokubi T, Kumakura I. Tongue pressure against hard palate during swallowing in post-stroke patients. Gerodontology. 2005;22:227–33. 30. Hirota N, Konaka K, Ono T, Tamine K, Kondo J, Hori K, Yoshimuta Y, Maeda Y, Sakoda S, Naritomi H. Reduced tongue pressure against the hard palate on the paralyzed side during swallowing predicts dysphagia in patients with acute stroke. Stroke. 2010;41:2982–4. 31. Tamine K, Ono T, Hori K, Kondoh J, Hamanaka S, Maeda Y. Age-related changes in tongue pressure during swallowing. J Dent Res. 2010;89:1097–101.
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40. Go¨rgu¨lu¨ S, Sag˘dic¸ D, Akin E, Karac¸ay S, Bulakbasi N. Tongue movements in patients with skeletal Class III malocclusions evaluated with real-time balanced turbo field echo cine magnetic resonance imaging. Am J Orthod Dentofacial Orthop. 2011;139: e405–14.
Megumi Hashimoto
DDS, PhD
Kazuko Igari DDS, PhD Soshi Hanawa
DDS, PhD
Ayumi Ito DDS, PhD Atsushi Takahashi Naoko Ishida
DDS, PhD
DDS
Shigeto Koyama DDS, PhD Takahiro Ono
DDS, PhD
Keiichi Sasaki DDS, PhD
ORIGINAL ARTICLE
Tongue Pressure During Swallowing in Adults with Down Syndrome and Its Relationship with Palatal Morphology Megumi Hashimoto • Kazuko Igari • Soshi Hanawa Ayumi Ito • Atsushi Takahashi • Naoko Ishida • Shigeto Koyama • Takahiro Ono • Keiichi Sasaki
•
Received: 11 November 2013 / Accepted: 18 April 2014 Ó Springer Science+Business Media New York 2014
Abstract In individuals with Down syndrome, hypotonicity of the tongue and an underdeveloped maxilla may lead to poor oral motor coordination, which adversely affects the oral phase of swallowing. This study aimed to evaluate the characteristics of pressure produced by the tongue against the hard palate during swallowing in individuals with Down syndrome. In addition, the relationship between tongue pressure and palatal morphology was examined. We studied nine adults with Down syndrome and ten healthy adults as controls. Tongue pressure while swallowing 5 mL water was recorded by a sensor sheet system with five measuring points attached to the hard palate. Palatal length, depth, width, curvature, and slope were measured by three-dimensional digital maxillary imaging. The order of onset of tongue pressure on the median line of the hard palate was the same in all participants, except for three with Down syndrome. The duration and maximal magnitude of tongue pressure on the median
line in nine participants with Down syndrome were significantly shorter and lower than those of controls. In participants with Down syndrome, significant positive correlations were observed between the duration of tongue pressure at the mid-median part of the hard palate and palatal depth and width, and between the duration and maximal magnitude of tongue pressure at the posteriormedian part and palatal length. These findings suggest that impaired tongue activity, poor tongue control, and constrained tongue motion due to a short and narrow palate contribute to swallowing difficulty in individuals with Down syndrome. Keywords Down syndrome Swallowing Tongue pressure Palatal morphology Deglutition Deglutition disorders
Introduction M. Hashimoto (&) S. Hanawa N. Ishida K. Sasaki Division of Advanced Prosthetic Dentistry, Tohoku University Graduate School of Dentistry, 4-1 Seiryo-machi, Aoba-ku, Sendai 980-8575, Japan e-mail: [email protected] M. Hashimoto K. Igari A. Ito A. Takahashi N. Ishida K. Sasaki Clinics of Dentistry for the Disabled, Tohoku University Hospital, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan S. Koyama Maxillofacial Prosthetics Clinic, Tohoku University Hospital, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan T. Ono Department of Prosthodontics, Gerodontology and Oral Rehabilitation, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka 565-0871, Japan
Down syndrome (DS), the most common chromosomal disorder, is characterized by developmental disabilities. Many individuals with DS have functional problems associated with mastication and swallowing [1–8], which are caused by neuromotor dysfunction, orofacial dysmorphology, dental abnormalities, and developmental delay [4, 9]. Underdevelopment of the maxilla, together with a narrow and short palate, has previously been described [10–12]. In addition, hypotonicity of the orofacial muscles, especially the tongue, is also common in DS [13, 14]. Consequently, individuals with DS have a hypotonic tongue in a relatively small oral cavity. These anatomical and neuromotor abnormalities may lead to poor oral motor coordination, such as open-mouth posture, tongue protrusion, and lack of stability of the mandible during mastication and swallowing
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[5, 9]. The tongue makes an important contribution to bolus transit during swallowing: contact pressure between the anterior tongue and the palate facilitates the beginning of the oral transport phase of swallowing [15], after which the tongue elevates a bolus to the palate, rolling and propelling it toward the pharynx by applying sequential anterior–posterior pressure [16]. Tongue pressure produced by contact between the hard palate and tongue is a major propulsive force in the transport of a food bolus toward the pharynx [17]. Inadequate generation of tongue pressure may indicate impaired tongue activity during swallowing. Stierwalt and Youmans [18] reported that reduced maximal isometric contraction of the tongue was evident in patients with oral dysphagia. Konaka et al. [19] have shown that the maximal magnitude of tongue pressure during swallowing in patients with dysphagia after stroke was lower than in those without dysphagia. They also reported that patients with dysphagia had a polyphasic pattern of tongue pressure, which suggested repetitive tongue movement as compensation for lower tongue pressure. Gisel et al. [1] reported that most 4- and 5-year-old children with DS protrude the tongue during swallowing, and they did not make the transition from infantile swallowing to the mature type of swallowing seen in agematched typically developing children. Smith et al. [20] reported that inadequate lip closure, impaired tongue movement, and lack of stability of the mandible were often observed during swallowing in adults with DS, although in their study the majority of participants were either edentulous or had very few teeth. The impairment of oral motor coordination, inadequate lip closure, and weak and impaired tongue movement make it difficult to acquire the basic functions of mastication and swallowing [8]. Difficulty in keeping food in the mouth [20], longer mastication time [2], reduced chewing frequency [7], and difficulty transferring a bolus [3] during eating and drinking have been observed in individuals with DS. Several studies have noted that anatomical abnormality of the oral cavity affected the oral phase of swallowing in individuals with DS [5, 9, 20, 21]. However, it is not clear how maxillary hypoplasia with a short and narrow palate influences tongue function during swallowing in individuals with DS. In more than half of children with DS, delayed initiation of the swallowing response and liquid aspiration were found in studies of swallowing function using videofluoroscopy [3, 22]. One report found that coughing during eating and drinking was observed in one half of adults with DS [20], which is suggestive of aspiration. As a result of swallowing difficulties lasting into adulthood, general health can be affected by respiratory illness or poor nutrition. Some therapies improve oral motor function, and this is considered to have a positive effect on development of mastication and swallowing in individuals with DS.
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Longitudinal observational studies have shown that early stimulating-plate therapy in physiotherapeutic practice in children with DS improves mouth posture and tongue position at rest [23, 24]. Subjective observational assessment of orofacial appearance has been widely used to evaluate mouth posture and tongue position in individuals with DS; however, this method cannot establish muscle strength and tongue function in a closed mouth. A more detailed, objective technique is needed to assess tongue function during swallowing. Electropalatography is a useful means of evaluating the temporal change of tongue contact position on the palate, but it does not measure contact pressure between the tongue and palate. Several studies that examine tongue pressure using pressure sensors have been conducted [16, 17, 25– 27]. Ono et al. [16] measured tongue pressure in healthy young adults using an experimental palatal plate that contained seven pressure sensors. They determined the normal pattern of tongue pressure production during swallowing by analyzing the time of onset, peak, and offset; duration; and maximal magnitude of tongue pressure. Based on this study, Hori et al. [28] developed a tactile sensor sheet with five measuring points that allows the measurement of tongue pressure during swallowing. The sensor sheet is sufficiently thin so that tongue pressure can be measured with little discomfort after a short familiarization period. This sensor sheet has been used to study not only elderly healthy volunteers but also patients after stroke [19, 29–31]. Therefore, we felt that the sensor sheet could be used to measure tongue pressure generation in individuals with DS who might have a limited ability to cooperate. We aimed to determine the characteristics of tongue pressure during swallowing in individuals with DS using the sensor sheet, and to compare timing of onset, peak, and offset; duration; maximal magnitude; and the integrated value of tongue pressure with those recorded in healthy individuals. In addition, we aimed to determine the effect of the characteristic palatal morphology of DS on tongue pressure. We hypothesized that duration, maximal magnitude, and integrated value of tongue pressure in adults with DS would be shorter and lower compared with those of healthy adult volunteers, and that the specific morphological changes to the palate in adults with DS would influence tongue pressure during swallowing.
Methods Participants The study population consisted of nine adults with DS. All were men with a mean (±standard deviation [SD]) age of 26.0 ± 5.9 years (range = 20–35 years) who were managed
M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome
regularly at the dental clinics of Tohoku University Hospital, Japan. Ten healthy volunteers matched for sex and age within 5 years of the participants were enrolled as controls (mean age = 26.0 ± 1.8 years; range = 24–30 years). Criteria for exclusion of participants with DS were a clinical history of prosthodontic treatment and loss of more than three teeth on either side. We also excluded potential participants with evidence of loss of occlusal support, namely, instability of the mandible, because of failure to achieve posterior occlusal contact, which could influence our measurements by impairing the normal mechanism of transporting a food bolus from the oral cavity to the pharynx [32]. All participants with DS had more than 24 natural teeth and consumed a normal diet. Criteria for exclusion of controls were a clinical history of deglutition disorder, orthodontic treatment, or temporomandibular disorder, any tooth loss except for the third molars, and occlusion abnormality. Written informed consent was obtained from the parents of participants with DS and from the controls. Oral agreement was obtained from each participant with DS with the capacity to do so. Conduct of the study was approved by the Ethics Committee of Tohoku University Graduate School of Dentistry (Nos. 22–28).
Fig. 1 Palatal view of the maxilla after attaching the sensor sheet in a participant with Down syndrome
Measurement of Tongue Pressure A tactile sensor system with a 0.1-mm-thick sensor sheet (Swallow scan; Nitta, Osaka, Japan) was used for the measurement of tongue pressure. The sensor sheet contains five measurement points (channels [Chs.] 1–5). According to the technique described by Hori et al. [28], three measurement points, Chs. 1–3, were placed along the median line of the palate. Ch. 1 was placed at the anterior-median part, Ch. 2 at the mid-median part, and Ch. 3 at the posterior-median part of the palate. The other two measurement points, Chs. 4 and 5, were placed at the right and left posterior-lateral part of the hard palate, respectively (Fig. 1). One sensor sheet was used for each participant; one of three sizes was selected to fit the palate. The sheet was directly attached to the palate with a sheet-type denture adhesive (Touch Correct II; Shionogi, Osaka, Japan), and a recording wire leading to a computer was passed through the oral vestibule without hindrance to occlusion. Before measurements were taken, the system was calibrated by applying negative pressure of a known value onto the sensor sheet using a vacuum pump attached to an air duct within the recording wire, mimicking positive pressure applied uniformly to each sensor. While taking measurements, the participant was seated in an upright position with feet on the floor. Each participant was asked to take 5 mL water (at 37 °C) into the mouth from a syringe and swallow when instructed. Five recordings of tongue pressure were made for each participant at intervals
Fig. 2 a Representative output signals of tongue pressure while 5 mL water is swallowed by a healthy participant. b Typical output of measurement of tongue pressure in Ch. 1
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of more than 1 min. The output signals of tongue pressure at Chs. 1–5 for each swallow were also recorded (Fig. 2a). The time of onset, peak, and offset; duration; maximal magnitude; and integrated value of tongue pressure for each waveform of Chs. 1–5 were analyzed later (Fig. 2b). Analyses of Palatal Morphology Alginate impressions of the participants’ maxillae were taken and a hard plaster cast was made. The following landmarks were marked on each cast: the incisive papilla (IP), the right and left hamular notches (HR, HL), and the deepest points of the gingival margin in the apical direction at the upper first molars on the right and left sides (MR, ML). A three-dimensional (3D) digital maxillary image was created from the cast on a personal computer by using a noncontact 3D digitizer with a resolution of 248 points/mm2 (NextEngine HD Pro; NextEngine, Inc., Santa Monica, CA, USA) and software (RapidWorks; Rapidform Japan, Tokyo, Japan). The 3D images of the maxilla and the landmarks on the cast were used to determine standardized measurements of the horizontal plane defined by IP, HR, and HL, and of the coronal plane, defined as the plane containing the line MR– ML perpendicular to the horizontal plane. The intersection point of the median palatine suture and the coronal plane (M) and the foot of the perpendicular line from M to the line MR–ML (MM) were also determined. Furthermore, 32 points that included MR, M, and ML were placed on the cross-sectional line of the palatal surface and the coronal plane to determine palatal curvature in the coronal section, with 15 points projected vertically from the points dividing the line segment MR–ML at regular intervals. In addition, 14 points were projected horizontally onto the right and left sides of the palate from the seven points dividing the line MM–M into eight equal portions. Thus, the following parameters were calculated for each participant: (1) palatal length: the distance between IP and the line HR–HL (Fig. 3a); (2) palatal depth: the distance between MM and M (Fig. 3b); (3) palatal width: the distance between MR and ML (Fig. 3b); and (4) palatal curvature (a): the curvature of the palate in the coronal section, defined as follows [33–35]. The curved line formed by 32 points on the palatal surface between MR and ML was approximated to a parabola: y = ax2 ? b. Perrier et al. [36] previously reported that a is described by the coefficient a from the equation for the parabola as 4 a ¼ pffiffiffiffiffiffi 3 j aj A high a value indicates a flat palate and a low a value indicates a sharp curved palate in the coronal section. The fifth parameter was palatal slope, defined as the angle made by the line IP–M with the horizontal plane (Fig. 3c).
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Fig. 3 Landmarks of palatal morphology in a three-dimensional (3D) digital image from the maxillary dental cast of a participant with Down syndrome (DS). a Palatal view. b Coronal view. c Sagittal view. IP, incisive papilla; HR, right hamular notch; HL, left hamular notch; MR, the deepest point of the gingival margin to the apical direction at the right first molar; ML, the deepest point of the gingival margin to the apical direction at the left first molar; M, intersection point of the median palatine suture and the coronal plane, defined as the plane containing the line MR–ML, perpendicular to the horizontal plane; MM, base of the perpendicular line from M to the line MR– ML. The horizontal plane is defined by IP, HR, and HL. Parameters of palatal morphology: (A), palatal length; (B), palatal depth; (C), palatal width; and (D), palatal slope
Statistical Analyses Differences in the timing of onset, peak, and offset of tongue pressure at five measurement points (Chs. 1–5) were compared using Friedman’s test, followed by the Wilcoxon signed-ranks test with Bonferroni’s correction as a post hoc analysis to test the differences between Chs. To examine whether there were differences in duration and maximal magnitude of tongue pressure among the five swallows in each of the five Chs., one-way repeated-measures analysis of variance (ANOVA) was performed for each group. The interaction and main effects in the
M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome
duration, maximal magnitude, and integrated value of tongue pressure in the five Chs. for the participants with DS and the controls were examined using two-way repeatedmeasures ANOVA, with the group as the independent variable and the measurement point as the dependent variable. In case of violation of assumption of sphericity, the degree of freedom was corrected using the Huynh-Feldt e. Significant interactions were analyzed by the simple maineffects test. We conducted Bonferroni’s test and the Welch test as post hoc analyses of the two-way repeated ANOVAs for Chs. and groups, respectively. Differences between the five parameters of palatal morphology were analyzed using the Mann–Whitney U test. Correlations between the duration and maximal magnitude of tongue pressure and the five parameters of palatal morphology were evaluated using Spearman’s correlation coefficients. Statistical significance was accepted as p \ 0.05. Data were analyzed using IBM SPSS ver. 21.0 (IBM Japan, Tokyo, Japan).
measurement point (F [3.40, 57.81] = 2.93, p = 0.035). The main effects between groups (F [1, 17] = 11.22, p = 0.004) and between measurement points (F [3.40, 57.81] = 19.75, p \ 0.001) were also significant. The duration of tongue pressure in participants with DS was significantly shorter than in controls at Chs. 1, 2, and 3 (p \ 0.01, Fig. 4a). Within the DS group, the duration of tongue pressure was significantly shorter at Chs. 1 and 2 (p \ 0.05) and Ch. 3 (p \ 0.01) than at Ch. 5. Within controls, the duration of tongue pressure at Ch. 1 was significantly longer than at Ch. 3 (p \ 0.05). In both groups, the duration of tongue pressure at Ch. 3 was significantly shorter than that at Chs. 4 and 5 (participants with DS, p \ 0.01; controls, p \ 0.05; Fig. 4a). Tongue pressure was significantly shorter on the median line of the palate (Chs. 1–3), especially in Ch. 1, in the participants with DS. Maximal Magnitude of Tongue Pressure
Three out the nine participants with DS showed partial pressure or no tongue pressure in Chs. 1–3. In the remaining six participants with DS, the order of onset of tongue pressure in Chs. 1–3 was from Ch. 1 to Ch. 2 and then Ch. 3. This sequential pattern of tongue pressure onset was the same as that in all controls. No significant difference was found in the timing of the onset, peak, and offset of tongue pressure in Chs. 1–5 between these six participants with DS and the controls.
A significant main effect was found for the maximal magnitude of tongue pressure between groups (F [1, 17] = 15.74, p = 0.001) and between measurement points (F [1.75, 29.71] = 9.76, p = 0.001). There was no significant relationship between group and measurement point (F [1.75, 29.71] = 1.36, p = 0.27). The maximal magnitude of tongue pressure in participants with DS was significantly lower than in controls at all measuring points, except for Ch. 4 (Chs. 1–3, p \ 0.01; Ch. 5, p \ 0.05; Fig. 4b). In participants with DS, the maximal magnitude of tongue pressure at Ch. 3 was significantly lower than at Ch. 4 (p \ 0.05) and at Ch. 5 (p \ 0.01). Within controls, the maximal magnitude of tongue pressure at Ch. 2 was significantly greater than at Ch. 3 (p \ 0.05; Fig. 4b). Overall, the maximal magnitude of tongue pressure on the palate was lower in participants with DS than in controls.
Inter- and Intra-individual Variability of Duration and Maximal Magnitude of Tongue Pressure
Integrated Values of Tongue Pressure
Results Order of Onset of Tongue Pressure
The pattern of tongue pressure in participants with DS varied considerably between individuals compared with controls. The duration and maximal magnitude of tongue pressure in participants with DS showed a trend toward shorter and lower values in Chs. 1–3 than those of controls. Analysis of intra-individual variability of the duration and maximal magnitude of tongue pressure found no significant difference among the five swallows at all five channels in both groups (participants with DS, p [ 0.05; controls, p [ 0.05). Duration of Tongue Pressure Analysis of the duration of tongue pressure showed a statistically significant relationship between group and
Analysis of the integrated value of tongue pressure showed a significant relationship between group and measurement point (F [3.05, 51.78] = 3.10, p = 0.034). The main effects between groups (F [1, 17] = 21.81, p \ 0.001) and between measurement points (F [3.05, 51.78] = 12.62, p \ 0.001) were also significant. The integrated values of tongue pressure in participants with DS were significantly lower than those in controls at all measurement points, except for Ch. 3 (p \ 0.01; Fig. 4c). In participants with DS, the integrated value at Ch. 3 was significantly lower than at Ch. 5 (p \ 0.05). Within controls, the integrated values at Chs. 1, 4, and 5 were significantly higher than those at Ch. 3 (p \ 0.01; Fig. 4c). In general, the integrated value of tongue
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M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome Fig. 4 Comparisons of the (a) duration, (b) maximal magnitude, and (c) integrated value of tongue pressure at each measurement point (Chs. 1–5) during swallowing in participants with DS and controls
pressure on the palate was lower in participants with DS, especially in Ch. 1. Correlations Between Duration and Maximal Magnitude of Tongue Pressure and Palatal Morphology The results of analyses of palatal morphology are shown in Table 1. Palatal length, width, and curvature in participants with DS were significantly lower than those in controls (palatal length, p \ 0.001; palatal width and curvature, p \ 0.01). There was no significant difference in palatal depth or slope between the groups.
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The duration of tongue pressure at Ch. 2 was significantly positively correlated with the palatal depth and width, and that at Ch. 3 was significantly positively correlated with palatal length in participants with DS (Table 2). In controls, there was no significant correlation between the duration of tongue pressure and palatal morphology. The maximal magnitude of tongue pressure at Ch. 3 was significantly positively correlated with palatal length, and at Ch. 5 it was significantly negatively correlated with palatal width in participants with DS (Table 3). In controls, the maximal magnitude of tongue pressure at Ch. 3 was significantly positively correlated with palatal width and curvature.
M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome Table 1 Palatal length, depth, width, curvature (a), and slope in participants with Down syndrome (DS) and controls Participants with DS (n = 9) Parameters
Median (IQR)
Controls (n = 10) Range
Median (IQR)
Range
p
Palatal length (mm)
39.11 (37.93–41.18)
36.38–42.36
45.80 (45.24–48.29)
42.47–49.77
\0.001
Palatal depth (mm)
12.79 (12.11–13.75)
11.91–14.60
12.74 (11.76–13.51)
8.46–15.07
0.568
Palatal width (mm)
29.72 (26.64–32.19)
22.47–41.44
35.94 (33.66–38.21)
31.06–43.16
0.007
Palatal curvature (a) Palatal slope (°)
1.69 (1.47–1.76)
1.31–2.23
2.00 (1.88–2.15)
1.81–2.73
0.003
29.40 (26.58–31.89)
21.64–36.14
27.77 (26.56–28.88)
16.10–31.55
0.191
Table 2 Spearman’s correlation coefficients (r) between the duration of tongue pressure and five parameters of palatal morphology in participants with Down syndrome (DS) and controls Group
Channel
Participants with DS (n = 9)
Ch. 1
0.43
0.52
0.52
0.47
Ch. 2
0.27
0.68*
0.78*
0.61
-0.17
Ch. 3
0.71*
-0.13
0.34
0.50
-0.55
Ch. 4
0.50
0.48
0.18
0.15
0.03
Controls (n = 10)
Palatal length
Palatal depth
Palatal width
Palatal curvature (a)
Palatal slope -0.05
Ch. 5
0.37
0.53
0.18
0.08
0.18
Ch. 1
-0.48
-0.12
-0.21
-0.09
0.39
Ch. 2 Ch. 3
0.10 0.25
-0.12 0.14
0.19 0.60
0.24 0.55
0.39 0.29
Ch. 4
0.08
0.06
-0.43
-0.26
-0.02
Ch. 5
0.53
-0.42
0.20
0.42
-0.47
* p \ 0.05
Table 3 Spearman’s correlation coefficients (r) between the maximal magnitude of tongue pressure and five parameters of palatal morphology in participants with Down syndrome (DS) and controls Group
Channel
Participants with DS (n = 9)
Ch. 1
0.22
0.27
0.20
0.35
Ch. 2
0.15
0.61
0.39
0.41
-0.17
Ch. 3
0.73*
-0.13
0.10
0.32
-0.65
Ch. 4
0.65
-0.03
-0.30
-0.08
-0.23
Ch. 5
0.50
-0.20
-0.73*
-0.48
-0.07
Ch. 1
0.16
-0.24
0.36
0.29
-0.32
Ch. 2 Ch. 3
0.19 -0.16
-0.26 -0.15
0.49 0.72*
0.49 0.67*
-0.16 -0.10
Controls (n = 10)
Palatal length
Palatal depth
Palatal width
Palatal curvature (a)
Palatal slope -0.22
Ch. 4
0.02
0.18
-0.03
-0.15
0.12
Ch. 5
-0.26
-0.04
0.15
0.13
-0.06
* p \ 0.05
Discussion This is the first study that examined the generation of tongue pressure in individuals with DS as a measure of tongue function during swallowing. Characteristic differences in the duration, maximal magnitude, and integrated value of tongue pressure between participants with DS and controls were found. In addition, tongue pressure was
correlated with the palatal length, depth, and width in participants with DS. We found partial tongue pressure or no tongue pressure at the measurement points on the median line in three of nine participants with DS. Therefore, we compared the order of onset of tongue pressure in the remaining six participants with DS with that recorded in the ten controls. Consistent with the study of Ono et al. [16], tongue
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M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome
pressure on the median line was generated from the anterior-median part to the mid-median part of the palate, and then to the posterior-median part in controls. This sequential pattern in the onset of tongue pressure in controls was the same as the six participants with DS. This finding, and the considerable interindividual differences observed, suggests that tongue function during swallowing varies widely in individuals with DS. Hypotonicity of the tongue could be one factor that causes shorter duration, lower maximal magnitude, and integrated value of tongue pressure in participants with DS. A decline in the duration and maximal magnitude of tongue pressure from anterior to posterior on the median line of the hard palate is a normal pattern of tongue pressure production in healthy individuals [16]. In controls, the duration and maximal magnitude of tongue pressure was essentially normal; however, there was no significant difference in the duration and maximal magnitude between the measurement points on the median line in participants with DS. Differences between participants with DS and controls could be explained by neuromotor dysfunction, abnormal palatal morphology, and maxillofacial structure, or both. Hamilton [37] proposed that tongue protrusion beyond the anterior teeth during articulation of alveolar sounds in adults with DS could result from difficulty in motor control of the tongue tip. Participants with DS in this study could swallow water with the mouth closed; however, the lower maximal magnitude and the shorter duration of tongue pressure at the anterior-median part of the palate (Ch. 1) in participants with DS indicated that the tongue tip might be positioned in a lower and more anterior position to the IP because of poor ability to control the tip. We also found that the length and width of the palate in participants with DS were significantly shorter than those in controls, but there was no significant difference in the depth of the palate between groups. These findings are in agreement with a study by Shapiro et al. [10]. The median value of the palatal curvature in the controls was 2.00 in our study, broadly comparable with the mean value of palatal curvature (1.93) in 11 healthy young men reported by Yunusova et al. [34]. The significantly lower value of the palatal curvature (median: 1.69) in participants with DS than in controls indicates that participants with DS had a steep curved palate in the coronal section. Some investigators have suggested that tongue movement during swallowing is related to maxillofacial morphology [38–40]. Go¨rgu¨lu¨ et al. [40] reported that the tongue tip was more anterior and the posterior border of contact between the tongue and the palate was more anterior during swallowing in individuals with class III malocclusion and maxillary retrognathism than in those with class I malocclusion. We found significant positive correlations between
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the duration and maximal magnitude of tongue pressure and the palatal length at the posterior-median part of the palate (Ch. 3). Although the position of the mandible related to the maxilla was unknown, these results suggest that a shorter palatal length was a factor in positioning the tongue anterior to the maxilla, which affected tongue pressure generation against the posterior-median part of the palate. Contact of the tongue tip with the lingual surface of the anterior teeth could be a way to seal the anterior oral cavity to adapt to an underdeveloped maxilla with a shorter palatal length in individuals with DS. Furthermore, we found significant positive correlations between the duration of tongue pressure and the palatal depth and width at the mid-median part of the palate (Ch. 2). Cheng et al. [39] reported that palatal depth and dental arch length, but not palatal width, were positively correlated with the magnitude of tongue movement during swallowing in healthy young adults. Unlike in healthy adults, a narrower palatal width is suspected to be the cause of constraint on tongue motion in participants with DS. In one participant with DS, who had the least palatal curvature (1.31), the narrowest width (22.47 mm), and the third shortest palatal length (37.79 mm) of all participants with DS, there was no tongue pressure on the median line (Chs. 1–3). Generally, the palatal morphology of individuals with DS deviates from normal more than that of healthy individuals. In addition, individuals with DS may have less capacity to adapt to abnormal palatal morphology than healthy individuals because of neuromotor dysfunction. Our study showed a significant correlation between tongue pressure during swallowing and palatal morphology in participants with DS; however, whether impaired tongue pressure causes palatal hypoplasia or whether abnormal palatal morphology constrains tongue movement is unclear. Further research is required to establish whether functional training of the tongue can promote normal growth of the palate, and how tongue pressure can change if orthodontic treatment is provided to expand the palate in individuals with DS. Our study had several limitations. First, the small sample size, the result of difficulty in recruiting participants with DS, limited the statistical power. Second, biased sampling, because of difficulty applying the experimental protocol to the entire population with DS, limits the generalizability of our findings. Depending on the extent of intellectual disability, individuals with DS appeared to find it difficult to tolerate the sensor sheet against their palate and to swallow when directed. Nonetheless, the technique could be used in most of the adults with DS who regularly visit our hospital for dental treatment or surveillance. Third, the sensor sheet did not fit the small palate of women with DS; a smaller sheet is required for use in children or women with DS.
M. Hashimoto et al.: Tongue Pressure During Swallowing in Down Syndrome
Although we investigated the relationship between tongue pressure and palatal morphology in participants with DS, tongue function during swallowing is affected by numerous factors such as the position of the mandible related to the maxilla, its stability, the size of the tonsils, and breathing through the mouth. Further studies are required to understand tongue function during swallowing and how it may be different in individuals with DS. To encourage development of oral motor skills associated with mastication and swallowing in individuals with DS, appropriate support—tailored to an individual’s level of understanding, capability, and compliance—is required. Evaluation of tongue function and palatal morphology can provide important information on the choice of proper food or to guide intervention. Therefore, tongue pressure measurements could be a useful guide for evaluating the therapeutic effects of interventions designed to improve tongue function in individuals with DS. In conclusion, impaired tongue activity, poor tongue control, and constrained tongue motion due to a short and narrow palate are likely to contribute to swallowing difficulties in individuals with DS. Acknowledgments We thank Dr. Nobue Goto, Dr. Hitomi Ando, and the staff at the Clinics of Dentistry for the Disabled, Tohoku University Hospital. We also thank all the participants in this study. Conflict of interest declare.
The authors have no conflicts of interest to
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Megumi Hashimoto
DDS, PhD
Kazuko Igari DDS, PhD Soshi Hanawa
DDS, PhD
Ayumi Ito DDS, PhD Atsushi Takahashi Naoko Ishida
DDS, PhD
DDS
Shigeto Koyama DDS, PhD Takahiro Ono
DDS, PhD
Keiichi Sasaki DDS, PhD
