Radiol Oncol 2018; 52(3): 250-256. doi: 10.2478/raon-2018-0032 250 research article Three-dimensional ultrasound evaluation of tongue posture and its impact on articulation disorders in preschool children with anterior open bite Sanda Lah Kravanja1, Irena Hocevar-Boltezar2, Maja Marolt Music3,4, Ana Jarc2, Ivan Verdenik5, Maja Ovsenik6 1 Dental Centre Dr Lah Kravanja, Bovec, Slovenia 2 Department of Otorhinolaryngology and Head & Neck Surgery, University Medical Centre Ljubljana, Ljubljana, Slovenia 3 Department of Radiology, Institute of Oncology Ljubljana, Ljubljana, Slovenia 4 Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia 5 Department of Obstetrics and Gynecology, University Medical Centre Ljubljana, Ljubljana, Slovenia 6 Department of Orthodontics and Dentofacial Orthopedics, Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia Radiol Oncol 2018; 52(3): 250-256. Received 7 July 2018 Accepted 13 July 2018 Correspondence to: Prof. Maja Ovsenik, D.M.D., Ph.D., Department of Orthodontics and Dentofacial Orthopaedics, Faculty of Medicine, University of Ljubljana, Vrazov trg 2, SI-1000 Ljubljana, Slovenia. E-mail: maja.ovsenik@mf.uni-lj.si Disclosure: No potential conflicts of interest were disclosed. Background. Tongue posture plays an important role in the etiology of anterior open bite (AOB) and articulation disorders, and is crucial for AOB treatment planning and posttreatment stability. Clinical assessment of tongue posture in children is unreliable due to anatomical limitations. The aim of the study was to present functional diagnostics us- ing three-dimensional ultrasound (3DUS) assessment of resting tongue posture in comparison to clinical assessment, and the associations between the improper tongue posture, otorhinolaryngological characteristics, and articulation disorders in preschool children with AOB. Patients and methods. A cross-sectional study included 446 children, aged 3–7 years, 236 boys and 210 girls, ex- amined by an orthodontist to detect the prevalence of AOB. The AOB was present in 32 children. The control group consisted of 43 children randomly selected from the participants with normocclusion. An orthodontist, an ear, nose and throat (ENT) specialist and a speech therapist assessed orofacial and ENT conditions, oral habits, and articulation disorders in the AOB group and control group. Tongue posture was also assessed by an experienced radiologist, us- ing 3DUS. The 3DUS assessment of tongue posture was compared to the clinical assessment of orthodontist and ENT specialist. Results. The prevalence of AOB was 7.2%. The AOB group and the control group significantly differed regarding improper tongue posture (p < 0.001), and articulation disorders (p < 0.001). In children without articulation disorders from both groups, the improper tongue posture occured less frequently than in children with articulation disorders (p < 0.001). After age adjustment, a statistical regression model showed that the children with the improper tongue posture had higher odds ratios for the presence of AOB (OR 14.63; p < 0.001) than the others. When articulation disor- ders were included in the model, these odds ratios for the AOB became insignificant (p = 0.177). There was a strong association between the improper tongue posture and articulation disorders (p = 0.002). The 3DUS detected the high- est number of children with improper resting tongue posture, though there was no significant difference between the 3DUS and clinical assessments done by orthodontist and ENT specialist. Conclusions. The 3DUS has proved to be an objective, non-invasive, radiation free method for the assessment of tongue posture and could become an important tool in functional diagnostics and early rehabilitation in preschool children with speech irregularities and irregular tongue posture and malocclusion in order to enable optimal condi- tions for articulation development. Key words: anterior open bite; tongue posture; three-dimensional ultrasound; prevalence; clinical evaluation; oral habits; articulation disorder Radiol Oncol 2018; 52(3): 250-256. Lah Kravanja S et al. / Three-dimensional US assessment of resting tongue posture 251 Introduction Anterior open bite (AOB) is defined as the absence of contact of the anterior teeth when the posterior teeth are in contact.1-3 It was established that hered- ity and several other factors (thumb and/or finger sucking, lip and tongue posture habits, impaired nasal breathing, and true skeletal growth abnor- malities) play an important role in the etiology of this type of malocclusion.4-7 The intrinsic vertical gap can cause difficulties in biting and chewing, affects the articulation and has unfavorable aes- thetic and psychological consequences. Since 80% of specific speech movements are made in the an- terior part of the mouth, it is not surprising that a relationship between articulation defects and mal- occlusion has long been assumed to exist.8 Among great diversity of malocclusions, AOB is the most common malocclusion associated with articulation disorders.9,10 The tongue is a muscular, largely movable or- gan in the oral cavity, important for many oral and oropharyngeal functions. The tongue resting pos- ture is believed to be even more important for the morphology of the growing jaws and the occlusion of the teeth than the tongue function during swal- lowing or speaking.8 Specifically, the total time of swallowing and speaking is too short to affect the equilibrium of the forces acting on the teeth and the growth of jaws. The resting tongue with its tone and pressure on the adjacent structures repre- sents one of the most important long-acting forces in the orofacial region. It has a great impact on the dentoalveolar development, dental occlusion, orofacial functions, the need for orthodontic treat- ment, and the posttreatment stability of the dental occlusion.3,10 An incorrect tongue posture has long been reported as a primary etiologic factor in the development of malocclusion, including AOB and articulation disorders.9,11 The clinical evaluation of the tongue resting posture is routinely performed during clinical ex- amination by ear, nose and throat (ENT) specialists and maxillofacial surgeons treating patients with clefts or orthognatic problems as well as by the orthodontists. However, clinical assessment of the tongue posture at rest without influencing and dis- turbing its natural posture is highly subjective in small growing children due to anatomical limita- tions.8 Despite its subjectivity, it remains the gold- en standard in clinical practise. There have been no reports in the literature on the reliability of clinical assessment of the resting tongue posture by differ- ent professionals for the same group of children. Three-dimensional ultrasonographic (3DUS) assessment of the tongue became recently an im- portant tool for imaging tongue size, shape and posture, recording functional tongue movements during swallowing, feeding and speech.12-16 With the use of 3DUS the objective resting tongue pos- ture can be displayed even in preschool children. The aim of the study was to present function- al diagnostics using 3DUS assessment of resting tongue posture in comparison to its clinical assess- ment, and the associations between the improper tongue posture, and AOB, orofacial, otorhinolaryn- gological characteristics, and articulation disorders in preschool children. Patients and methods The study protocol was approved by the Republic of Slovenia National Medical Ethics Committee (protocol No. 96/04/13). The parents of all included children signed an informed consent for their and their children participation in the study. Patients In the first part of the survey the prevalence of AOB and articulation disorders was established by a cross-sectional epidemiological study in children attending kindergartens in municipality Tolmin. In total, 446 preschool children (236 boys, 211 girls), aged 3 to 7 years, were included. The children with AOB (AOB group) and their parents were invited to participate in the second part of the study. The control group was recruited from the rest of the examined children without AOB. Seventy children without AOB were rando- mely selected and invited to further participate in the study as control group. Patient examination procedures In the first part of the study, all children were ex- amined by the same orthodontist (SLK) during the kindergarten visits to detect AOB and articulation disorders. The parents gave their assessment of na- sal breathing, possible articulation disorders and the necessity for speech therapy in their children. In the second part of the study, all AOB and control group children were examined at the or- thodontic clinic of the Community Dental Health Centre (Tolmin, Slovenia). During the intraoral examination the dental status, functional and mor- phological malocclusions were registered accord- Radiol Oncol 2018; 52(3): 250-256. Lah Kravanja S et al. / Three-dimensional US assessment of resting tongue posture252 ing to the method by Ovsenik et al.8 Alginate im- pressions and wax bite registrations were obtained and dental casts were prepared in the ortholab for documentation. The tongue posture at rest was re- corded. All AOB and control group children were exam- ined by an experienced ENT specialist (IHB) and a speech therapist (AJ). The clinical ENT examina- tion was performed with special emphasis on the resting tongue posture. In the case of an upper res- piratory infection, the child was reinvited for the examination when he/she was healthy. The speech therapist performed a three-position test for articulation disorders and registered pos- sible articulation disorders. Three-dimensional US examination The children from both groups were invited for a 3DUS examination of the tongue posture by an experienced radiologist (MMM), Institute of Oncology in Ljubljana, with the use of the ul- trasound system Voluson 730 Expert (General Electrics Healthcare, Kretztechnik, Zipf Austria) with a 3D convex transducer (RAB 2–5 MHz, GEH). Each child was seated in the dental chair, head positioned in the Frankfort horizontal line, parallel to the floor, and fixed with a strap. The 3D convex tranducer was coated with an aqueous con- tact transmission gel and positioned on the skin of the mouth floor in the midsagittal line. Each child was asked to be relaxed and to remain still for 15 seconds; no instructions were given for the tongue posture. The recording procedure was repeated twice, using the following parameters: 55-65-de- gree view, mechanical index 0.8, thermical index 0.3. The acquired data were transferred to a per- sonal computer and visualized using the 4D View software version 5.0 (General Electrics Healthcare, Waukesha, Wisconsin). Referential 3D reconstruc- tions obtained from 10 children without malocclu- sion in deciduous dentition were then used to com- pare the tongue posture for each child according to the method presented by Volk et al.17 The correct resting tongue posture was recorded when the tip of the tongue was on the palate behind the upper incisors (Figure 1). In the improper rest- ing tongue posture, the 3DUS displayed the tip of the tongue to be low on the mouth floor (Figure 2) according to the method by Volk et al.17 The US im- age of the tongue on the palate showed convexity of its dorsum (Figure 1), while when on the mouth floor the tongue dorsum showed a distinctive con- cavity with a central groove (Figure 2). Statistical analysis All the collected data were analysed using the R statistical package (www.R-project.org). The da- ta were analysed and compared using χ²-test or Fisher’s exact test, t-test or nonparametric Mann- Whitney test. The multiple logistic regression model was used for the assessments of factors possibly associated with AOB. The results of the FIGURE 1. The US images of the child’s resting tongue posture on the palate: sagittal view (A); antero - posterior (transverse) view (B); vertical view (C); 3D reconstruction of the tongue showing a convexity of the tongue dorsum (D). D = Dorsum, R = Radix, T = Tip of the tongue FIGURE 2. The US images of the child’s resting tongue posture on the floor of the mouth: sagittal view (A); anteroposterior (transverse) view (B); vertical view (C); 3D reconstruction of the tongue (D) showing a a central groove (G) on the tongue dorsum. D = Dorsum, R = Radix, T = Tip of the tongue A A B B C C D D Radiol Oncol 2018; 52(3): 250-256. Lah Kravanja S et al. / Three-dimensional US assessment of resting tongue posture 253 clinical assessment of the resting tongue posture performed by an orthodontist and an ENT special- ist were compared with the results of US imaging using McNemar’s test. The reliability of the clinical evaluation was calculated. The level of statistical significance was set at 0.05, and 95% confidence in- tervals were used. Results AOB was found in 32 subjects (7.2%). The compari- son of the general data and the parents’ assessment of possible child’s articulation disorders for the AOB children and the rest of the pediatric popula- tion without AOB are presented in Table 1. There were significant differences between the groups in the occurrence of articulation disorders, and neces- sity for speech therapy. The parents of 61.4% children out of the 70 ran- domly selected were willing to allow them to par- ticipate in the second part of the study. Thus, the control group consisted of 43 children. All AOB and control group children underwent further examinations by the orthodontist, the ENT specialist, the speech therapist and the radiologist. The orthodontist found improper tongue posture on the floor of the mouth in 20 (62.5%) children from the AOB group, and in 9 (20.9%) children from the control group. During the ENT examination, 12 AOB children and 14 control group children were found to have an upper airway infection. They were invited again for the examination three weeks later. All AOB children and only two control group children had a control ENT examination. Therefore, the find- ings of the ENT examination of the AOB group could only be considered for further analysis. In the AOB group, the ENT examination detected low tongue posture in 23 subjects (71.8%), incompetent lip closure in 22 subjects (68.8%), nasal breathing impairment in 19 subjects (59.4%), and hypertrofic adenoid/status post adenoidectomy in 17 subjects (53.1%). The 3DUS assessment of the resting tongue posture showed the improper tongue posture on the mouth floor in 81.3% of the AOB children and in 25.6% of the control group children. When the results of the US-assessed tongue posture (26 chil- dren with improper posture) were compared with the ENT clinical assessment (23 subjects with im- proper posture) and clinical orthodontic assess- ment (20 children with improper posture), no sig- nificant differences were detected (p = 0.549 and p = 0.180, respectively; Figure 3). The speech therapist and orthodontist found articulation disorders in 84.4% of AOB children and in 23.2% of control group children. In the AOB group, the most frequently detected articulation disorders were sigmatism (present in 25 children) and rhotacism (present in 16 children). Sixteen children had multiple articulation disorders. In the control group, there were 8 children with sigma- FIGURE 3. Comparison of the assessment of the resting tongue posture by the clinical orthodontic examination, clinical ENT examination, and 3DUS examination in the AOB children. TABLE 1. Comparison of the general data and the parents’ assessment of the child’s nasal breathing, the possible articulation disorders and the necessity for speech therapy between the group of children with anterior open bite (AOB) (N = 32) and the rest of the pediatric population without anterior open bite (N = 414) Parameter AOB (N = 32) Without AOB (N = 414) P Age (years)1 4.9 (1.0) 5.0 (0.9) 0.548 Nasal breathing, day2 31 (96.9%) 348 (84.1%) 0.056 Nasal breathing, night 29 (90.6%) 350 (84.5%) 0.382 Articulation disorder (parental assessment) 27 (84.4%) 108 (26.1%) < 0.001 Necessity for speech therapy 13 (40.6%) 99 (23.9%) 0.018 1 For numerical variables mean and SD are given; 2 for categorical number and percentage Radiol Oncol 2018; 52(3): 250-256. Lah Kravanja S et al. / Three-dimensional US assessment of resting tongue posture254 tism and 6 children with rhotacism; 7 children had multiple articulation disorders. In the AOB group and control group together, there were 37 children with articulation disorders. Among them there were 31 children with resting tongue posture on the floor of the mouth. In 38 children without articulation disorders, there were only 6 children with improper resting tongue pos- ture (p < 0.001). Table 2 compares the AOB and the control group children with respect to the general data, the resting posture of the tongue and the occurrence of articulation disorders detected by orthodontist and speech therapist. There was a significant difference between the groups in age, resting tongue posture, and occurence of articulation disorders. There was a significant difference in age be- tween the AOB group and control group. For further analysis, age adjustment was performed. The significant variables were included into two multiple logistic regression models: model 1 (age, improper tongue posture) and model 2 (age, im- proper tongue posture, presence of articulation disorders). The results for model 1 showed that the improper resting tongue posture (according to the US examination) and the presence of AOB were associated. The children with the tongue posture on the floor of the mouth had higher odds ratios for the presence of AOB (OR 14.63, 95% CI 4.08–52.39, and p < 0.001). When articulation dis- orders were included (model 2), the odds ratios for the presence of AOB became insignificant for the children with improper resting tongue posture (OR 3.16, 95% CI 0.59–16.79, and p = 0.177). This was likely a consequence of a strong association between the tongue posture and articulation dis- orders. Apparently, it is the presence of articula- tion disorders, strongly associated with improper tongue posture, that has the most significant cor- relation with the presence of AOB (OR 13.79, 95% CI 2.56–74.23, and p = 0.002). Discussion Clinical examination of the tongue posture and function is an important part of functional diag- nostics in orthodontics and dentofacial orthopae- dics as well as in the field of ENT. However, it is difficult to get objective findings of tongue posture during clinical examination in small children be- cause of their cooperation and anatomical charac- teristics of the orofacial area.17 According to Graber et al.18 the assessment of tongue posture during clinical examination should be performed in the physiological resting position of the mandible and the examiner should slightly open the lips of the examinee to register the posture of the tongue in the oral cavity. However, even a slightest touch of the lips could represent a stimulus for the examinee to drop the tongue to the mouth floor and in the direction of the touched lips.16,19 Many studies investigated tongue function during swallowing and speech by using radio- cinematography,20,21 magnetic resonance,22 and 2-dimensional ultrasonography,19,23 while tongue posture has been evaluated by using lateral cepha- lograms and computed tomography.24 The disad- vantage of these diagnostic procedures is radiation exposure, which contraindicates these methods to be used in small still growing children and disa- bles frequent repetitions of the proposed methods. Ultrasonography is a noninvasive method and is widely used in many fields in medicine, obstet- rics, gynecology, perinatology, and pediatrics.25-27 Three-dimensional ultrasonography greatly im- proved and nowadays permits acquisition of high resolution images. It was also used in the studies in the orofacial area (e.g. in adult patients after partial resection of the tongue).28,29 However, data about 3D surface morphology of anatomically normal but diversely postured tongues at rest in growing children have only been performed in the field of orthodontics.17 TABLE 2. Comparison of the general data, ultrasound-assessed resting tongue posture, and the prevalence of articulation disorders between the anterior open bite group (N = 32) and the control group (N = 43) Parameter AOB group (N = 32) Control group (N = 43) p Male gender1 17 (53%) 20 (46%) 0.571 Age (years)2 4.9 (1.0) 4.3 (0.3) < 0.001 Articulation disorder (speech therapist’s assessment) 27 (84%) 10 (23%) < 0.001 Improper resting tongue posture (3DUS) 26 (81%) 11 (26%) 0.001 1 For categorical variables number and percentage is given; 2 for numerical mean and SD. AOB = anterior open bite; 3D US = three-dimensional ultrasound Radiol Oncol 2018; 52(3): 250-256. Lah Kravanja S et al. / Three-dimensional US assessment of resting tongue posture 255 In the present study, 3D ultrasonography was used for the first time in the assessment of tongue posture in the early stage of growth and develop- ment in preschool children with articulation disor- ders and AOB. Furthermore, in this study the clini- cal assessment of the tongue posture under stand- ard conditions was performed independently by two different specialists, the experts in functional diagnostics of the orofacial area, by the ENT special- ist and by the orthodontist. Their assessments were compared to the 3DUS examination performed by an experienced radiologist. The results of all three examiners using different methods were found to be in agreement (Mc Nemar’s test, p = 0.180 and p = 0.549, respectively) (Figure 3). However, the 3DUS method objectively revealed the largest num- ber of children with low tongue posture, which proved the validity of this diagnostic tool. To the best of our knowledge, this study was the first one to evaluate the reliability between the clinical ENT and orthodontic assessment of the tongue posture, and compared to the 3DUS assessment. With the use of 3DUS, 81.2% of the children with AOB were found to have improper tongue posture on the mouth floor, while in the control group sub- jects, the irregular tongue posture was registered only in 25.6% of the examined children (McNemar’s test, p < 0.001). The interpretation of our findings confirmed that improper tongue posture on the mouth floor is prevalent in children with AOB. Furthermore, the present study found similar results of the irregular tongue posture in control group subjects (25,6 %) without malocclussion as reported previously in the study by Volk et al.17 The two studies demonstrated very clearly that 3DUS can be used for the assessment of tongue posture in growing children. The main advantage of the 3DUS method is its non-invasive character, which enabels that repetitions of the examination can frequently be performed. The results suggested that besides the known risk factors (long bottle feeding, finger sucking) the resting tongue posture on the mouth floor is crucial for the development of AOB. The important factors for the development of AOB can be impaired na- sal breathing and enlarged adenoids which were detected in almost two thirds of the AOB group. Unfortunately, a comparison with the control group was not possible because a considerable number of children from control group had upper airway in- fection at the time of ENT examination. The oede- ma of the nasal mucosa and the size of adenoids as a consequence of viral infection influenced the patency of the nose, possibility of nasal breathing, lip closure and resting posture of the tongue in the oral cavity. Therefore, the signs of the infection pre- vented a comparison of the AOB group and control group at the time when the ENT examination took place. On the other hand, when we compared the data on child’s nasal breathing during day according to the parents’ report between the children with AOB and the other children without AOB, the difference was close to the significant values. This result sug- gested that the cause for improper tongue posture might be an insufficient patency of the nose in the time of jaws’ development resulting in a malocclu- sion. The majority of the children with AOB (84.4%) had articulation disorders in comparison to the control group children (23.2%). One of the reasons for such a high number of children with articula- tion disorders may be a result of individual stage of growth and development of articulation. At the age of 5-6 years late maturation articulation disorders can still be observed.11 However, when children from both groups were observed, the children with- out articulation disorders had a statistically signifi- cantly lower percentage of the improper tongue posture (15.8%) than the children with articulation disorders (83.8%). This strong association between AOB, improper resting tongue posture, and articu- lation disorders was found to be one of the main clinically relevant results of this study. It can there- fore be concluded that these factors are important risk factors for articulation disorders of the sounds performed in the anterior part of the mouth. From this point of view, a precise functional diagnostics is very important in the assessment of early treatment needs for AOB in the deciduous dentition in order to implement interceptive and preventative actions, and to provide optimal bal- anced condition in the oral cavity for proper articu- lation development. The 3DUS assessment of tongue posture was found to be an important and valuable tool for the objective assessment of resting tongue posture not only in the etiology of malocclusion and articula- tion disorders, but also to further objectify the ef- ficiency of early orthodontic treatment, assessment of the success of treatment, and consequently to evaluate successful long-term oral rehabilitation. The main advantage of the proposed method is its non-invasive character. 3DUS proved to be the most valid and reliable method to assess improper rest- ing tongue posture as it most objectively identified the highest number of children with improper rest- ing posture of the tongue in the oral cavity. From Radiol Oncol 2018; 52(3): 250-256. Lah Kravanja S et al. / Three-dimensional US assessment of resting tongue posture256 the clinician’s point of view, it is also relatively sim- ple, quick, repeatable and child-friendly method. Conclusions This study demonstrated that 3DUS is an objective, reliable, non-invasive, radiation free, non time- consuming, and child-friendly diagnostic tool for the assessment of tongue posture in small children. Furthermore, 3DUS identified the highest number of incorrect tongue postures, which was highly re- lated to articulation disorders in preschool children with malocclusion. Therefore, every clinical exami- nation of orofacial functions in preschool children should be focused on proper resting tongue pos- ture. The child and his/her parents should get the early information about the correct resting tongue posture in the mouth. In this way, an optimal con- dition in the oral cavity for proper tongue matura- tion and articulation development can be created. 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