Predictors of sleep disordered breathing in children: the PANIC study

Predictors of sleep disordered breathing in children: the PANIC study Summary Objective We studied longitudinally the associations of craniofacial morphology, mouth breathing, orthodontic treatment, and body fat content with the risk of having and developing sleep disordered breathing (SDB) in childhood. We hypothesized that deviant craniofacial morphology, mouth breathing, and adiposity predict SDB among children. Materials and methods The participants were 412 children 6–8 years of age examined at baseline and 329 children aged 9–11 years re-examined at an average 2.2-year follow-up. An experienced orthodontist evaluated facial proportions, dental occlusion, soft tissue structures, and mode of breathing and registered malocclusions in orthodontic treatment. Body fat percentage was assessed by dual-energy X-ray absorptiometry and SDB symptoms by a questionnaire. Results Children with SDB more likely had convex facial profile, increased lower facial height, mandibular retrusion, tonsillar hypertrophy, and mouth breathing at baseline and convex facial profile, mandibular retrusion, and mouth breathing at follow-up than children without SDB at these examinations. Male gender and body adiposity, mouth breathing, and distal molar occlusion at baseline were associated with SDB later in childhood. Adipose tissue under the chin, mandibular retrusion, vertically large or normal throat and malocclusion in orthodontic treatment at baseline predicted developing SDB during follow-up of among children without SDB at baseline. Limitations We could not conduct polysomnographic examinations to define sleep disturbances. Instead, we used a questionnaire filled out by the parents to assess symptoms of SDB. Conclusions The results indicate that among children, deviant craniofacial morphology, mouth breathing, body adiposity, and male gender seem to have implications in the pathophysiology of SDB. Introduction Sleep disordered breathing (SDB), a spectrum of symptoms ranging from habitual snoring to obstructive sleep apnea (OSA) (1) is a chronic and progressive condition that is becoming more common worldwide (2). The prevalence of habitual snoring is 28–44% in adults (3) and 7–25% in children and adolescents (4–6), whereas that of OSA is 2–4% in adults (3) and 1–3% in children and adolescents (4, 5, 7, 8). Although SDB is nowadays recognized more sensitively than earlier, it remains a highly under-diagnosed condition. We have reported earlier that 10% of children 6–8 years of age from a general population have SDB (9). It is important to identify children at increased risk of SDB to prevent its health consequences, such as cardiovascular disease, metabolic disturbances, delayed somatic growth, depression, and decreased quality of life (10). Adiposity is known to be a major risk factor for SDB in adults (11), but it has also been associated with SDB in some studies among children (4, 12, 13). Our previous study revealed that tonsillar hypertrophy, facial convexity, and crossbite but not adiposity were associated with increased risk of SDB in a general population of children 6–8 years of age (9). Other studies have also shown that abnormal craniofacial structures, such as adenotonsillar hypertrophy (10, 14), mandibular retrusion, a steep mandibular plane, a vertical direction of facial growth, and distal occlusion, are related to the increased risk of SDB among children (15). On the other hand, orthodontic treatment modalities, such as maxillary expansion (16, 17) and functional treatments advancing mandible (18, 19), may play a role in the prevention of SDB among children. There are few prospective population-based studies on the predictors of SDB among children. We therefore investigated the associations of craniofacial structures, mouth breathing, malocclusions in orthodontic treatment, and body fat content at the age of 6–8 years with the risk of SDB on average 2.2 years later in a population sample of children. We hypothesized that children with SDB symptoms could be identified in early childhood and further, that the craniofacial growth may modify the risk factors for SDB. Materials and methods Study design and study population The present analyses are based on the data of the Physical Activity and Nutrition in Children (PANIC) Study, which is an ongoing physical activity and dietary intervention study in a population sample of children from the city of Kuopio, Finland. Altogether 736 children 6–8 years of age who started the first grade in primary schools of Kuopio in 2007–2009 were invited to participate in the study (20). Of the 736 invited children, 512 (70%) participated in the baseline examinations. Of these 512 children, 440 (86%) also attended in the 2-year follow-up examinations. Complete data for the present analyses were obtained from 329 children. The study group consisted of 161 (48.9%) girls and 168 (51.1%) boys, at the baseline mean (standard deviation, SD) age of the children being 7.6 (0.4) years and after 2.2 year follow-up 10.1 (0.5) years. The study protocol was approved by the Research Ethics Committee of the Hospital District of Northern Savo. All participating children and their parents gave their informed written consent. Assessment of craniofacial structures and dental occlusion Craniofacial structures and dental occlusion were clinically evaluated by a standard orthodontic screening method by an experienced orthodontist (TI). The occlusion was assessed according to the modified method of Björk et al. (21) in the intercuspal position. The recorded variables included molar occlusion (distal, normal, or mesial), overjet (mm), overbite (mm), crowding, and spacing per dental arch (≥2 mm), anterior and lateral open bite (≥2 mm) as well as crossbite and scissors bite. The shape of the palate was visually defined as wide, normal, or narrow. The existence of adipose tissue under the chin was examined by viewing the lateral profile of the child to asses if there was a visible amount of submandibular fat. The facial profile was also assessed visually (convex, normal, concave, vertical anterior facial dimension). To assess the airway space between the tonsils the children were asked to breathe through their nose, which relaxes the pharynx and palatal area. The tonsils were considered hypertrophied, if there was a space of 1 cm or less between the tonsils in visual inspection. The definition corresponds to Classes 3–4 described by Brodsky (22). Soft palatal morphology was classified using a clinical examination on maximal mouth opening and tongue protrusion in the seated position, as described by Mallampati et al. (23). With Mallampati Classes I and II, the morphology was classified as vertically normal/large throat and with Classes III and IV as vertically restricted throat. Dominance of mouth breathing was assessed visually during the clinical examination. Previous or ongoing orthodontic treatment was checked from dental recordings and classified according to the most prevalent treatment modalities in Finnish children among the studied age groups: Quad helix, head gear, or other (mostly eruption guidance appliance). Noteworthy, if an examination showed treatment need, a child was referred to an appropriate professional (i.e., dentist, orthodontist, physician). Assessment of body composition Body fat percentage was measured the children having voided, being in light clothing and in supine position, and after removing all metal objects using the Lunar Prodigy Advance® dual-energy X-ray absorptiometry device (GE Medical Systems, Madison, Wisconsin, USA). Assessment of sleep, SDB, and associated factors The questions in our sleep questionnaire were based on an established questionnaire that has been used to screen for sleep disturbances and SDB (24) and modified in the present study for the parents to fill out on behalf of their children. The parents were asked to answer to questions regarding the quantity and quality of sleep, symptoms of SDB, upper airway infections, adenotonsillectomy, and other operative treatments. SDB symptom was defined as witnessed breathing pauses (apneas) (sometimes, usually, or always/almost always) and/or frequent (most of the sleeping time or frequently) and/or loud (quite loudly, loudly, or extremely loudly) snoring and/or nocturnal mouth breathing (usually or always/almost always) observed by the parents. In other words, if the child had one or more of above-mentioned symptoms, he/she was defined as having SDB. Statistical methods The Chi-square statistics or the Fisher’s Exact Test was used to compare the prevalence of abnormal craniofacial structures and dental malocclusions between children with SDB and those without it. The Student’s t-test was used to compare body fat percentage between girls and boys and between children with SDB and those without it. Multiple logistic regression analysis using a stepwise entering selection procedure was used to study the associations of craniofacial abnormalities (no versus yes), dental malocclusions (no versus yes), mouth breathing (no versus yes), malocclusion in orthodontic treatment (no versus yes), and body fat percentage (per 1 standard deviation increase) at the age of 6–8 years with the risk of having or developing SDB on average 2.2 years later after adjustment for sex. Associations with P values of <0.05 were considered statistically significant. All statistical analyses were performed using the IBM SPSS Statistics®, Version 21 (IBM Corp., Armonk, New York, USA). Results Characteristics of children The mean (standard deviation, SD) body fat percentage at the age of 6–8 years was 22.3 (7.9) among girls and 17.6 (8.0) among boys (P < 0.001 for difference) and at the age of 9–11 25.2 (8.6) and 21.7 (9.5), respectively (P = 0.001). Of all 329 children, 33 (10.8%) had SDB at baseline and 38 (11.6%) had SDB at 2-year follow-up. SDB disappeared in 16 (4.8%) children during 2-year follow-up. It appeared in 21 (7.1%) out of 296 children without SDB at baseline during 2-year follow-up. At baseline, children with SDB were more likely to have convex facial profile, increased lower facial height, mandibular retrusion, tonsillar hypertrophy, and mouth breathing than those without SDB (Table 1). At 2-year follow-up, children with SDB were more likely to have convex facial profile, mandibular retrusion, and mouth breathing than those without it (Table 1). Table 1. Characteristics of children with SDB and those without it at baseline and at 2.2-year follow-up. Children examined at baseline (n = 329) Children examined at 2.2-year follow-up (n = 329) Children with SDB (n = 33) Children without SDB (n = 296) P value Children with SDB (n = 38) Children without SDB (n = 291) P value Distal molar occlusion 12 (36.4) 87 (29.4) 0.408 13 (34.2) 68 (23.4) 0.145 Crossbite 7 (21.2) 35 (11.8) 0.163a 5 (13.2) 24 (8.2) 0.356a Open bite 3 (9.4) 9 (3.0) 0.101a 0 (0) 3 (1.0) 1.000a Crowding 16 (48.5) 151 (51.0) 0.783 13 (34.2) 127 (43.6) 0.269 Scissors bite 1 (3.0) 3 (1.0) 0.346a 3 (7.9) 8 (2.7) 0.122a Convex facial profile 18 (54.5) 93 (31.4) 0.008 20 104 (35.7) 0.043 Increased lower facial height 12 (36.4) 59 (19.9) 0.030 (52.6)12 (31.6) 58 (19.9) 0.099 Mandibular retrusion 16 (48.5) 82 (27.7) 0.013 20 (52.6) 93 (32.0) 0.012 Maxillary retrusion 0 (0) 6 (2.0) 1.000a 3 (7.9) 6 (2.1) 0.073a Decreased palatal width 7 (21.2) 34 (11.5) 0.158a 8 (21.1) 31 (10.7) 0.103a Tonsillar hypertrophy 8 (24.2) 22 (7.4) 0.005a 6 (15.8) 19 (6.5) 0.053a Vertically restricted throatb 17 (51.5) 130 (43.9) 0.405 10 (26.3) 90 (30.9) 0.561 Mouth breathing 9 (27.3) 18 (6.1) <0.001a 7 (18.4) 12 (4.1) 0.003a Malocclusion in orthodontic treatment 3 (9.1) 22 (7.4) 0.727a 10 (26.3) 52 (17.9) 0.211 Thick neck 3 (9.1) 44 (14.9) 0.598a 1 (2.6) 4 (1.4) 0.461a Adipose tissue under the chin 9 (27.3) 96 (33.4) 0.474 11 (28.9) 47 (16.3) 0.056 Fat percentagec 19.2 (8.6) 20.0 (8.2) 0.608c 25.5 (10.1) 23.1 (9.1) 0.135c Children examined at baseline (n = 329) Children examined at 2.2-year follow-up (n = 329) Children with SDB (n = 33) Children without SDB (n = 296) P value Children with SDB (n = 38) Children without SDB (n = 291) P value Distal molar occlusion 12 (36.4) 87 (29.4) 0.408 13 (34.2) 68 (23.4) 0.145 Crossbite 7 (21.2) 35 (11.8) 0.163a 5 (13.2) 24 (8.2) 0.356a Open bite 3 (9.4) 9 (3.0) 0.101a 0 (0) 3 (1.0) 1.000a Crowding 16 (48.5) 151 (51.0) 0.783 13 (34.2) 127 (43.6) 0.269 Scissors bite 1 (3.0) 3 (1.0) 0.346a 3 (7.9) 8 (2.7) 0.122a Convex facial profile 18 (54.5) 93 (31.4) 0.008 20 104 (35.7) 0.043 Increased lower facial height 12 (36.4) 59 (19.9) 0.030 (52.6)12 (31.6) 58 (19.9) 0.099 Mandibular retrusion 16 (48.5) 82 (27.7) 0.013 20 (52.6) 93 (32.0) 0.012 Maxillary retrusion 0 (0) 6 (2.0) 1.000a 3 (7.9) 6 (2.1) 0.073a Decreased palatal width 7 (21.2) 34 (11.5) 0.158a 8 (21.1) 31 (10.7) 0.103a Tonsillar hypertrophy 8 (24.2) 22 (7.4) 0.005a 6 (15.8) 19 (6.5) 0.053a Vertically restricted throatb 17 (51.5) 130 (43.9) 0.405 10 (26.3) 90 (30.9) 0.561 Mouth breathing 9 (27.3) 18 (6.1) <0.001a 7 (18.4) 12 (4.1) 0.003a Malocclusion in orthodontic treatment 3 (9.1) 22 (7.4) 0.727a 10 (26.3) 52 (17.9) 0.211 Thick neck 3 (9.1) 44 (14.9) 0.598a 1 (2.6) 4 (1.4) 0.461a Adipose tissue under the chin 9 (27.3) 96 (33.4) 0.474 11 (28.9) 47 (16.3) 0.056 Fat percentagec 19.2 (8.6) 20.0 (8.2) 0.608c 25.5 (10.1) 23.1 (9.1) 0.135c Data are numbers (percentages) and P-values are from Chi-square test. aP values from Fisher’s exact test. bDefined as Classes III or IV as described by Mallampati et al. (22). cData are means (standard deviations) and P values are from Student’s t-test. View Large Table 1. Characteristics of children with SDB and those without it at baseline and at 2.2-year follow-up. Children examined at baseline (n = 329) Children examined at 2.2-year follow-up (n = 329) Children with SDB (n = 33) Children without SDB (n = 296) P value Children with SDB (n = 38) Children without SDB (n = 291) P value Distal molar occlusion 12 (36.4) 87 (29.4) 0.408 13 (34.2) 68 (23.4) 0.145 Crossbite 7 (21.2) 35 (11.8) 0.163a 5 (13.2) 24 (8.2) 0.356a Open bite 3 (9.4) 9 (3.0) 0.101a 0 (0) 3 (1.0) 1.000a Crowding 16 (48.5) 151 (51.0) 0.783 13 (34.2) 127 (43.6) 0.269 Scissors bite 1 (3.0) 3 (1.0) 0.346a 3 (7.9) 8 (2.7) 0.122a Convex facial profile 18 (54.5) 93 (31.4) 0.008 20 104 (35.7) 0.043 Increased lower facial height 12 (36.4) 59 (19.9) 0.030 (52.6)12 (31.6) 58 (19.9) 0.099 Mandibular retrusion 16 (48.5) 82 (27.7) 0.013 20 (52.6) 93 (32.0) 0.012 Maxillary retrusion 0 (0) 6 (2.0) 1.000a 3 (7.9) 6 (2.1) 0.073a Decreased palatal width 7 (21.2) 34 (11.5) 0.158a 8 (21.1) 31 (10.7) 0.103a Tonsillar hypertrophy 8 (24.2) 22 (7.4) 0.005a 6 (15.8) 19 (6.5) 0.053a Vertically restricted throatb 17 (51.5) 130 (43.9) 0.405 10 (26.3) 90 (30.9) 0.561 Mouth breathing 9 (27.3) 18 (6.1) <0.001a 7 (18.4) 12 (4.1) 0.003a Malocclusion in orthodontic treatment 3 (9.1) 22 (7.4) 0.727a 10 (26.3) 52 (17.9) 0.211 Thick neck 3 (9.1) 44 (14.9) 0.598a 1 (2.6) 4 (1.4) 0.461a Adipose tissue under the chin 9 (27.3) 96 (33.4) 0.474 11 (28.9) 47 (16.3) 0.056 Fat percentagec 19.2 (8.6) 20.0 (8.2) 0.608c 25.5 (10.1) 23.1 (9.1) 0.135c Children examined at baseline (n = 329) Children examined at 2.2-year follow-up (n = 329) Children with SDB (n = 33) Children without SDB (n = 296) P value Children with SDB (n = 38) Children without SDB (n = 291) P value Distal molar occlusion 12 (36.4) 87 (29.4) 0.408 13 (34.2) 68 (23.4) 0.145 Crossbite 7 (21.2) 35 (11.8) 0.163a 5 (13.2) 24 (8.2) 0.356a Open bite 3 (9.4) 9 (3.0) 0.101a 0 (0) 3 (1.0) 1.000a Crowding 16 (48.5) 151 (51.0) 0.783 13 (34.2) 127 (43.6) 0.269 Scissors bite 1 (3.0) 3 (1.0) 0.346a 3 (7.9) 8 (2.7) 0.122a Convex facial profile 18 (54.5) 93 (31.4) 0.008 20 104 (35.7) 0.043 Increased lower facial height 12 (36.4) 59 (19.9) 0.030 (52.6)12 (31.6) 58 (19.9) 0.099 Mandibular retrusion 16 (48.5) 82 (27.7) 0.013 20 (52.6) 93 (32.0) 0.012 Maxillary retrusion 0 (0) 6 (2.0) 1.000a 3 (7.9) 6 (2.1) 0.073a Decreased palatal width 7 (21.2) 34 (11.5) 0.158a 8 (21.1) 31 (10.7) 0.103a Tonsillar hypertrophy 8 (24.2) 22 (7.4) 0.005a 6 (15.8) 19 (6.5) 0.053a Vertically restricted throatb 17 (51.5) 130 (43.9) 0.405 10 (26.3) 90 (30.9) 0.561 Mouth breathing 9 (27.3) 18 (6.1) <0.001a 7 (18.4) 12 (4.1) 0.003a Malocclusion in orthodontic treatment 3 (9.1) 22 (7.4) 0.727a 10 (26.3) 52 (17.9) 0.211 Thick neck 3 (9.1) 44 (14.9) 0.598a 1 (2.6) 4 (1.4) 0.461a Adipose tissue under the chin 9 (27.3) 96 (33.4) 0.474 11 (28.9) 47 (16.3) 0.056 Fat percentagec 19.2 (8.6) 20.0 (8.2) 0.608c 25.5 (10.1) 23.1 (9.1) 0.135c Data are numbers (percentages) and P-values are from Chi-square test. aP values from Fisher’s exact test. bDefined as Classes III or IV as described by Mallampati et al. (22). cData are means (standard deviations) and P values are from Student’s t-test. View Large Risk factors for SDB Male gender, distal molar occlusion, mouth breathing, and increased body fat percentage at baseline were associated with increased risk of having SDB at 2.2-year follow-up (Table 2). Mouth breathing was the strongest baseline predictor of SDB at 2.2-year follow-up. Children with mouth breathing at baseline had a 4.4-times higher risk of SDB at 2.2-year follow-up than those without it. Table 2. Baseline predictors for having SDB at 2.2-year follow-up among all 329 children. Odds ratio 95% confidence interval P value Male gender 2.2 1.0–4.6 0.042 Distal molar occlusion 2.2 1.1–4.6 0.032 Mouth breathing 4.4 1.7–11.4 0.002 1 SD increase in body fat percentage 1.5 1.1–2.1 0.015 Odds ratio 95% confidence interval P value Male gender 2.2 1.0–4.6 0.042 Distal molar occlusion 2.2 1.1–4.6 0.032 Mouth breathing 4.4 1.7–11.4 0.002 1 SD increase in body fat percentage 1.5 1.1–2.1 0.015 Data are from stepwise logistic regression models, the effect of gender was considered in each step. Only statistically significant determinants are given. View Large Table 2. Baseline predictors for having SDB at 2.2-year follow-up among all 329 children. Odds ratio 95% confidence interval P value Male gender 2.2 1.0–4.6 0.042 Distal molar occlusion 2.2 1.1–4.6 0.032 Mouth breathing 4.4 1.7–11.4 0.002 1 SD increase in body fat percentage 1.5 1.1–2.1 0.015 Odds ratio 95% confidence interval P value Male gender 2.2 1.0–4.6 0.042 Distal molar occlusion 2.2 1.1–4.6 0.032 Mouth breathing 4.4 1.7–11.4 0.002 1 SD increase in body fat percentage 1.5 1.1–2.1 0.015 Data are from stepwise logistic regression models, the effect of gender was considered in each step. Only statistically significant determinants are given. View Large Mandibular retrusion, a vertically large or normal throat, adipose tissue under the chin and malocclusion in orthodontic treatment at baseline were associated with increased risk of developing SDB during 2.2-year follow-up (Table 3). Malocclusion in orthodontic treatment was the strongest baseline predictor of developing SBD during 2.2-year follow-up. Children who had a malocclusion in orthodontic treatment at baseline had a 5.0 times higher risk of SBD than those without it. Table 3. Baseline predictors for incident SBD at 2.2-year follow-up among 296 children who had no SDB at baseline. Odds ratio 95% confidence interval P value Mandibular retrusion 3.4 1.3–8.9 0.012 Vertically restricted throata 0.2 0.1–0.7 0.011 Adipose tissue under the chin 2.8 1.1–7.2 0.034 Malocclusion in orthodontic treatment 5.0 1.3–18.4 0.016 Odds ratio 95% confidence interval P value Mandibular retrusion 3.4 1.3–8.9 0.012 Vertically restricted throata 0.2 0.1–0.7 0.011 Adipose tissue under the chin 2.8 1.1–7.2 0.034 Malocclusion in orthodontic treatment 5.0 1.3–18.4 0.016 Data are from stepwise logistic regression models, the effect of gender was considered in each step. Only statistically significant determinants are given. aDefined as Classes III or IV as described by Mallampati et al. (22). View Large Table 3. Baseline predictors for incident SBD at 2.2-year follow-up among 296 children who had no SDB at baseline. Odds ratio 95% confidence interval P value Mandibular retrusion 3.4 1.3–8.9 0.012 Vertically restricted throata 0.2 0.1–0.7 0.011 Adipose tissue under the chin 2.8 1.1–7.2 0.034 Malocclusion in orthodontic treatment 5.0 1.3–18.4 0.016 Odds ratio 95% confidence interval P value Mandibular retrusion 3.4 1.3–8.9 0.012 Vertically restricted throata 0.2 0.1–0.7 0.011 Adipose tissue under the chin 2.8 1.1–7.2 0.034 Malocclusion in orthodontic treatment 5.0 1.3–18.4 0.016 Data are from stepwise logistic regression models, the effect of gender was considered in each step. Only statistically significant determinants are given. aDefined as Classes III or IV as described by Mallampati et al. (22). View Large Discussion The present longitudinal study showed that already at the age of 6–8 years there are certain morphological and functional features that can predict developing SDB at the age of 9–11 years. Especially higher body adiposity and mouth breathing, as well as distal molar occlusion seemed to predispose to the development of SDB already in childhood. Furthermore, as in adults (25), male gender also increased the risk of SDB. Adipose tissue under the chin, mandibular retrusion, vertically normal/large throat, and malocclusion in orthodontic treatment were associated with developing SDB during the 2.2 year follow-up. Adenotonsillar hypertrophy is the most common risk factor for pediatric SDB (10, 14). The volume of the adenoid and tonsils increases from birth to the age of 12 years, the peak of their size proportional to the skeletal structures being at the age of 5–6 years (10). Even though nasal resistance decreases from 9 to 13 years of age, there is a transient prepubertal increase in the resistance, a phenomenon suggested to result from hormonal changes (26). According to Papaioannou et al. (27), during the first 8 years of life the pharyngeal lymphoid tissue is likely to be exposed to external microbial stimuli that promote cellular proliferation. In line, pediatric SDB is most common in pre-school and early school years (28). We found that tonsillar hypertrophy was common among children with SDB and that mouth breathing, usually co-existing with tonsillar hypertrophy, at the age of 6–8 years was associated with increased risk of SDB 2.2 years later. Interestingly, children with vertically large or normal throat had increased risk for SDB. The same children also tended to have hypertrophied tonsils more often than those with vertically restricted throat. This may indicate that those children had developed a lowered position of the tongue to improve their breathing, which is in line with the results of the classical study of Linder-Aronson (29). Further, Suri et al. showed that abnormal palatal morphology significantly predicted a poor outcome of the treatment of SDB with adenotonsillectomy and suggested that a delay in treating the hypertrophied adenoid and tonsils may promote abnormal craniofacial growth, leading to residual SDB (30). Malocclusion in orthodontic treatment at baseline was associated with increased risk of developing SDB during 2.2-year follow-up in our study. As found in previous studies deviant craniofacial morphology, such as retrognathic mandible, reduced width of maxillary dental arch, and anterior open bite are associated with SDB among children (31–33). In our study, children with SDB were more likely to have facial convexity, mandibular retrusion and increased facial height than those without it. Furthermore, distal molar occlusion at the age of 6–8 years predicted SDB 2.2 years later. These malocclusions are usually diagnosed and early orthodontic treatment is initiated at that age in Finland. The impact of different treatment modalities would require further examination since, basically, early orthodontic treatment is thought to prevent SDB in adulthood by modifying the deviant craniofacial morphology (17, 18). Adiposity has been observed to be an important risk factor for developing SDB in children (13, 25). A recent study showed that especially increased amount of visceral fat was associated with more serious manifestations of SDB in a population sample of children (34). Parallel to the results of these studies, we found that a higher body fat percentage at the age of 6–8 years was associated with a higher risk of having SBD 2.2 years later and further, adipose tissue under the chin was associated with increased risk of developing SDB during 2.2-year follow-up. The mechanism by which adiposity predisposes to SDB may be the mass loading of upper airway and respiratory muscles (5) causing alterations to the structure and function of these muscles, the reduction of chest wall compliance, changes in respiratory drive and the impairment of functional residual capacity, all of which increase the risk of upper airway obstruction (25). It is alarming that overweight and obesity are becoming more common in children and adolescents in many developed countries (35). In Finland, 10% of children and 26% of adolescents have been found to be overweight (36). In fact, obese children have been observed to have an increased risk of persistent SDB even after adenotonsillectomy, which is the first line treatment for pediatric SDB (25). In children, the associations of overweight and obesity with SDB may not be straightforward, and the relationship may be modified by other factors, such as age, ethnicity, and craniofacial morphology (25). Generally, sleep disorders are suggested to be more prevalent in boys (37) and like in adults, boys to have more SDB compared with girls (38). There are also studies to show no gender difference in the prevalence of SDB (39, 40). Further, some questionnaire-based studies show boys to have more SDB compared with girls (38, 41). The present study showed male gender to increase the risk of SDB. A strength of our study is that we used a population-based sample of children to study the longitudinal associations of body fat percentage, dental malocclusions, other craniofacial abnormalities, mouth breathing, and orthodontic treatment with SDB. We assessed body fat percentage using DXA that is a reliable and valid measure of body fat content (20). Limitations Because of the epidemiological nature of the study we could not conduct demanding polysomnographic examinations to define sleep disturbances. Instead, we used a questionnaire filled out by the parents to assess SDB symptoms. Some parents may have been unaware of their children’s sleeping pattern that may have caused inaccuracy in reporting. However, our sleep questionnaire was based on an established Finnish questionnaire (24) that is a widely used method to assess SDB (42). After follow-up we had complete data of 64% of the children studied at baseline. The burden of numerous medical, nutritional, physical, psychological, and dental examinations may have caused the quite large proportion of drop-outs. We did not examine the size of the adenoids, because in this age group the only ethical and reliable method would have been magnetic resonance imaging that was not feasible because of the epidemiological nature of the study. However, as the hypertrophy of the adenoid and tonsils typically coexist and indicate the amount of lymphoid tissue in the pharynx, it may not be relevant to consider them as different conditions. Further, we did not have the opportunity for a rhinomanometric examination to examine nasal resistance and the size of the nasopharyngeal area. Finally, the observational design of our study makes it difficult to draw conclusions about causal relationships between the exposure and outcome variables and given the large confidence intervals, the study results need to be interpreted with caution. Conclusions Deviant craniofacial morphology, mouth breathing, adiposity, and male gender may predict SDB in childhood. These findings are useful in identifying growing children at increased risk of developing SDB. Children with these features could be candidates for early intervention to prevent the progression of SDB later in life. Funding The PANIC Study has been financially supported by grants from the Ministry of Social Affairs and Health of Finland (090/KTL/TE/2008; 148/KTL/TE/2009; 178/THL/TE/2010; 178/THL/TE/2011), the Ministry of Education and Culture of Finland (105/627/2006; 104/626/2008; 121/627/2009; 108/627/2010; 55/627/2011; OKM/48/626/2013), the University of Eastern Finland, the Finnish Innovation Fund Sitra (5451031/1), the Social Insurance Institution of Finland (22/26/2008), the Finnish Cultural Foundation (00090566; 00100516), the Juho Vainio Foundation, the Foundation for Pediatric Research, the Paulo Foundation, the Paavo Nurmi Foundation, the Diabetes Research Foundation, and the Kuopio University Hospital (EVO 5031343), the Yrjö Jahnsson Foundation (66779), Jenny and Antti Wihuri Foundation and Päivikki and Sakari Sohlberg Foundation. Conflict of Interest None to declare. References 1. Li , H.Y. and Lee , L.A . ( 2009 ) Sleep-disordered breathing in children . Chang Gung Medical Journal , 32 , 247 – 257 . Google Scholar PubMed 2. Bradley , T.D. and Floras , J.S . ( 2009 ) Obstructive sleep apnoea and its cardiovascular consequences . Lancet (London, England) , 373 , 82 – 93 . Google Scholar CrossRef Search ADS PubMed 3. Young , T. , Palta , M. , Dempsey , J. , Skatrud , J. , Weber , S. and Badr , S . ( 1993 ) The occurrence of sleep-disordered breathing among middle-aged adults . The New England Journal of Medicine , 328 , 1230 – 1235 . Google Scholar CrossRef Search ADS PubMed 4. Ng , D.K. , Lam , Y.Y. , Kwok , K.L. and Chow , P.Y . ( 2004 ) Obstructive sleep apnoea syndrome and obesity in children . Hong Kong Medical Journal , 10 , 44 – 48 . Google Scholar PubMed 5. Ng , D.K. , Chow , P.Y. , Chan , C.H. , Kwok , K.L. , Cheung , J.M. and Kong , F.Y . ( 2006 ) An update on childhood snoring . Acta Paediatrica (Oslo, Norway: 1992) , 95 , 1029 – 1035 . Google Scholar CrossRef Search ADS PubMed 6. Hultcrantz , E. and Löfstrand Tideström , B . ( 2009 ) The development of sleep disordered breathing from 4 to 12 years and dental arch morphology . International Journal of Pediatric Otorhinolaryngology , 73 , 1234 – 1241 . Google Scholar CrossRef Search ADS PubMed 7. Ali , N.J. , Pitson , D.J. and Stradling , J.R . ( 1993 ) Snoring, sleep disturbance, and behaviour in 4-5 year olds . Archives of Disease in Childhood , 68 , 360 – 366 . Google Scholar CrossRef Search ADS PubMed 8. Ali , N.J. , Pitson , D. and Stradling , J.R . ( 1994 ) Natural history of snoring and related behaviour problems between the ages of 4 and 7 years . Archives of Disease in Childhood , 71 , 74 – 76 . Google Scholar CrossRef Search ADS PubMed 9. Ikävalko , T. et al. ( 2012 ) Craniofacial morphology but not excess body fat is associated with risk of having sleep-disordered breathing–the PANIC Study (a questionnaire-based inquiry in 6-8-year-olds) . European Journal of Pediatrics , 171 , 1747 – 1752 . Google Scholar CrossRef Search ADS PubMed 10. Dayyat , E. , Kheirandish-Gozal , L. , Gozal , D . ( 2007 ) Childhood obstructive sleep apnea: one or two distinct disease entities ? Sleep Medicine Clinics , 2 , 433 – 444 . Google Scholar CrossRef Search ADS PubMed 11. Leinum , C.J. , Dopp , J.M. and Morgan , B.J . ( 2009 ) Sleep-disordered breathing and obesity: pathophysiology, complications, and treatment . Nutrition in Clinical Practice , 24 , 675 – 687 . Google Scholar CrossRef Search ADS PubMed 12. Marcus , C.L. , Curtis , S. , Koerner , C.B. , Joffe , A. , Serwint , J.R. and Loughlin , G.M . ( 1996 ) Evaluation of pulmonary function and polysomnography in obese children and adolescents . Pediatric Pulmonology , 21 , 176 – 183 . Google Scholar CrossRef Search ADS PubMed 13. Verhulst , S.L. , Van Gaal , L. , De Backer , W. and Desager , K . ( 2008 ) The prevalence, anatomical correlates and treatment of sleep-disordered breathing in obese children and adolescents . Sleep Medicine Reviews , 12 , 339 – 346 . Google Scholar CrossRef Search ADS PubMed 14. Arens , R. et al. ( 2003 ) Upper airway size analysis by magnetic resonance imaging of children with obstructive sleep apnea syndrome . American Journal of Respiratory and Critical Care Medicine , 167 , 65 – 70 . Google Scholar CrossRef Search ADS PubMed 15. Flores-Mir , C. , Korayem , M. , Heo , G. , Witmans , M. , Major , M.P. and Major , P.W . ( 2013 ) Craniofacial morphological characteristics in children with obstructive sleep apnea syndrome: a systematic review and meta-analysis . Journal of the American Dental Association (1939) , 144 , 269 – 277 . Google Scholar CrossRef Search ADS PubMed 16. Guilleminault , C. and Li , K.K . ( 2004 ) Maxillomandibular expansion for the treatment of sleep-disordered breathing: preliminary result . The Laryngoscope , 114 , 893 – 896 . Google Scholar CrossRef Search ADS PubMed 17. Ashok , N. , Varma , N.K. , Ajith , V.V. and Gopinath , S . ( 2014 ) Effect of rapid maxillary expansion on sleep characteristics in children . Contemporary Clinical Dentistry , 5 , 489 – 494 . Google Scholar CrossRef Search ADS PubMed 18. Hänggi , M.P. , Teuscher , U.M. , Roos , M. and Peltomäki , T.A . ( 2008 ) Long-term changes in pharyngeal airway dimensions following activator-headgear and fixed appliance treatment . European Journal of Orthodontics , 30 , 598 – 605 . Google Scholar CrossRef Search ADS PubMed 19. Villa , M.P. , Miano , S. and Rizzoli , A . ( 2012 ) Mandibular advancement devices are an alternative and valid treatment for pediatric obstructive sleep apnea syndrome . Sleep & Breathing , 16 , 971 – 976 . Google Scholar CrossRef Search ADS 20. Eloranta , A.M. et al. ( 2012 ) Dietary factors associated with overweight and body adiposity in Finnish children aged 6-8 years: the PANIC Study . International Journal of Obesity (2005) , 36 , 950 – 955 . Google Scholar CrossRef Search ADS PubMed 21. Björk , A. , Krebs , B. and Solow , B . ( 1964 ) A method for epidemiological registration of malocclusion . Acta Odontologica Scandinavica , 22 , 27 – 41 . Google Scholar CrossRef Search ADS PubMed 22. Brodsky , L . ( 1989 ) Modern assessment of tonsils and adenoids . Pediatric Clinics of North America , 36 , 1551 – 1569 . Google Scholar CrossRef Search ADS PubMed 23. Mallampati , S.R. et al. 1985 A clinical sign to predict difficult tracheal intubation: a prospective study . Canadian Anaesthetists’ Society Journal , 32 , 429 – 434 . Google Scholar CrossRef Search ADS PubMed 24. Partinen , M. and Gislason , T . ( 1995 ) Basic Nordic Sleep Questionnaire (BNSQ): a quantitated measure of subjective sleep complaints . Journal of Sleep Research , 4 , 150 – 155 . Google Scholar CrossRef Search ADS PubMed 25. Kohler , M.J. and van den Heuvel C.J . ( 2008 ) Is there a clear link between overweight/obesity and sleep disordered breathing in children ? Sleep Medicine Reviews , 12 , 347 – 361 . Google Scholar CrossRef Search ADS PubMed 26. Crouse , U. , Laine-Alava , M.T. and Warren , D.W . ( 2000 ) Nasal impairment in prepubertal children . American Journal of Orthodontics and Dentofacial Orthopedics , 118 , 69 – 74 . Google Scholar CrossRef Search ADS PubMed 27. Papaioannou , G. , Kambas , I. , Tsaoussoglou , M. , Panaghiotopoulou-Gartagani , P. , Chrousos , G. and Kaditis A.G . ( 2013 ) Age-dependent changes in the size of adenotonsillar tissue in childhood: implications for sleep-disordered breathing . The Journal of Pediatrics , 162 , 269 – 74.e4 . Google Scholar CrossRef Search ADS PubMed 28. Corbo , G. M. et al. ( 2001 ) Snoring in 9- to 15-year-old children: risk factors and clinical relevance . Pediatrics , 108 , 1149 – 1154 . Google Scholar CrossRef Search ADS PubMed 29. Linder-Aronson , S . ( 1970 ) Adenoids. Their effect on mode of breathing and nasal airflow and their relationship to characteristics of the facial skeleton and the denition. A biometric, rhino-manometric and cephalometro-radiographic study on children with and without adenoids . Acta Otolaryngologica , 265 , 1 – 132 . 30. Suri , J.C. , Sen , M.K. , Venkatachalam , V.P. , Bhool , S. , Sharma , R. , Elias , M. and Adhikari , T . ( 2015 ) Outcome of adenotonsillectomy for children with sleep apnea . Sleep Medicine , 16 , 1181 – 1186 . Google Scholar CrossRef Search ADS PubMed 31. Löfstrand-Tideström , B , Thilander , B , Ahlqvist-Rastad , J. , Jakobsson , O. and Hultcrantz , E . ( 1999 ) Breathing obstruction in relation to craniofacial and dental arch morphology in 4-year-old children . European Journal of Orthodontics , 21 , 323 – 332 . Google Scholar CrossRef Search ADS PubMed 32. Marino , A. , Malagnino , I. , Ranieri , R. , Villa , M.P. and Malagola , C . ( 2009 ) Craniofacial morphology in preschool children with obstructive sleep apnoea syndrome . European Journal of Paediatric Dentistry , 10 , 181 – 184 . Google Scholar PubMed 33. Pirilä-Parkkinen , K. , Pirttiniemi , P. , Nieminen , P. , Tolonen , U. , Pelttari , U. and Löppönen , H . ( 2009 ) Dental arch morphology in children with sleep-disordered breathing . European Journal of Orthodontics , 31 , 160 – 167 . Google Scholar CrossRef Search ADS PubMed 34. Bixler , E.O. et al. ( 2016 ) Natural history of sleep disordered breathing in prepubertal children transitioning to adolescence . The European Respiratory Journal , 47 , 1402 – 1409 . Google Scholar CrossRef Search ADS PubMed 35. Kipping , R.R. , Jago , R. and Lawlor , D.A . ( 2008 ) Obesity in children. Part 1: Epidemiology, measurement, risk factors, and screening . BMJ (Clinical research ed.) , 337 , a1824 . Google Scholar CrossRef Search ADS PubMed 36. Vuorela , N. , Saha , M.T. and Salo , M . ( 2009 ) Prevalence of overweight and obesity in 5- and 12-year-old Finnish children in 1986 and 2006 . Acta Paediatrica (Oslo, Norway: 1992) , 98 , 507 – 512 . Google Scholar CrossRef Search ADS PubMed 37. Paavonen , E.J. et al. ( 2000 ) Sleep problems of school-aged children: a complementary view . Acta Paediatrica (Oslo, Norway: 1992) , 89 , 223 – 228 . Google Scholar CrossRef Search ADS PubMed 38. Gill , A.I. , Schaughency , E. and Galland , B.C . ( 2012 ) Prevalence and factors associated with snoring in 3-year olds: early links with behavioral adjustment . Sleep Medicine , 13 , 1191 – 1197 . Google Scholar CrossRef Search ADS PubMed 39. Goodwin , J.L. et al. ; Tucson Children’s Assessment of Sleep Apnea Study . 2003 Symptoms related to sleep-disordered breathing in white and Hispanic children: the Tucson Children’s Assessment of Sleep Apnea Study . Chest , 124 , 196 – 203 . Google Scholar CrossRef Search ADS PubMed 40. Liukkonen , K. , Virkkula , P. , Aronen , E.T. , Kirjavainen , T. and Pitkäranta , A . ( 2008 ) All snoring is not adenoids in young children . International Journal of Pediatric Otorhinolaryngology , 72 , 879 – 884 . Google Scholar CrossRef Search ADS PubMed 41. Ersu , R. et al. ( 2004 ) Prevalence of snoring and symptoms of sleep-disordered breathing in primary school children in Istanbul . Chest , 126 , 19 – 24 . Google Scholar CrossRef Search ADS PubMed 42. Kapuniai , L.E. , Andrew , D.J. , Crowell , D.H. and Pearce , J.W . ( 1988 ) Identifying sleep apnea from self-reports . Sleep , 11 , 430 – 436 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2017. Published by Oxford University Press on behalf of the European Orthodontic Society. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The European Journal of Orthodontics Oxford University Press

Loading next page...
 
/lp/ou_press/predictors-of-sleep-disordered-breathing-in-children-the-panic-study-MtYQmBChdY
Publisher
Oxford University Press
Copyright
© The Author(s) 2017. Published by Oxford University Press on behalf of the European Orthodontic Society. All rights reserved. For permissions, please email: journals.permissions@oup.com
ISSN
0141-5387
eISSN
1460-2210
D.O.I.
10.1093/ejo/cjx056
Publisher site
See Article on Publisher Site

Abstract

Summary Objective We studied longitudinally the associations of craniofacial morphology, mouth breathing, orthodontic treatment, and body fat content with the risk of having and developing sleep disordered breathing (SDB) in childhood. We hypothesized that deviant craniofacial morphology, mouth breathing, and adiposity predict SDB among children. Materials and methods The participants were 412 children 6–8 years of age examined at baseline and 329 children aged 9–11 years re-examined at an average 2.2-year follow-up. An experienced orthodontist evaluated facial proportions, dental occlusion, soft tissue structures, and mode of breathing and registered malocclusions in orthodontic treatment. Body fat percentage was assessed by dual-energy X-ray absorptiometry and SDB symptoms by a questionnaire. Results Children with SDB more likely had convex facial profile, increased lower facial height, mandibular retrusion, tonsillar hypertrophy, and mouth breathing at baseline and convex facial profile, mandibular retrusion, and mouth breathing at follow-up than children without SDB at these examinations. Male gender and body adiposity, mouth breathing, and distal molar occlusion at baseline were associated with SDB later in childhood. Adipose tissue under the chin, mandibular retrusion, vertically large or normal throat and malocclusion in orthodontic treatment at baseline predicted developing SDB during follow-up of among children without SDB at baseline. Limitations We could not conduct polysomnographic examinations to define sleep disturbances. Instead, we used a questionnaire filled out by the parents to assess symptoms of SDB. Conclusions The results indicate that among children, deviant craniofacial morphology, mouth breathing, body adiposity, and male gender seem to have implications in the pathophysiology of SDB. Introduction Sleep disordered breathing (SDB), a spectrum of symptoms ranging from habitual snoring to obstructive sleep apnea (OSA) (1) is a chronic and progressive condition that is becoming more common worldwide (2). The prevalence of habitual snoring is 28–44% in adults (3) and 7–25% in children and adolescents (4–6), whereas that of OSA is 2–4% in adults (3) and 1–3% in children and adolescents (4, 5, 7, 8). Although SDB is nowadays recognized more sensitively than earlier, it remains a highly under-diagnosed condition. We have reported earlier that 10% of children 6–8 years of age from a general population have SDB (9). It is important to identify children at increased risk of SDB to prevent its health consequences, such as cardiovascular disease, metabolic disturbances, delayed somatic growth, depression, and decreased quality of life (10). Adiposity is known to be a major risk factor for SDB in adults (11), but it has also been associated with SDB in some studies among children (4, 12, 13). Our previous study revealed that tonsillar hypertrophy, facial convexity, and crossbite but not adiposity were associated with increased risk of SDB in a general population of children 6–8 years of age (9). Other studies have also shown that abnormal craniofacial structures, such as adenotonsillar hypertrophy (10, 14), mandibular retrusion, a steep mandibular plane, a vertical direction of facial growth, and distal occlusion, are related to the increased risk of SDB among children (15). On the other hand, orthodontic treatment modalities, such as maxillary expansion (16, 17) and functional treatments advancing mandible (18, 19), may play a role in the prevention of SDB among children. There are few prospective population-based studies on the predictors of SDB among children. We therefore investigated the associations of craniofacial structures, mouth breathing, malocclusions in orthodontic treatment, and body fat content at the age of 6–8 years with the risk of SDB on average 2.2 years later in a population sample of children. We hypothesized that children with SDB symptoms could be identified in early childhood and further, that the craniofacial growth may modify the risk factors for SDB. Materials and methods Study design and study population The present analyses are based on the data of the Physical Activity and Nutrition in Children (PANIC) Study, which is an ongoing physical activity and dietary intervention study in a population sample of children from the city of Kuopio, Finland. Altogether 736 children 6–8 years of age who started the first grade in primary schools of Kuopio in 2007–2009 were invited to participate in the study (20). Of the 736 invited children, 512 (70%) participated in the baseline examinations. Of these 512 children, 440 (86%) also attended in the 2-year follow-up examinations. Complete data for the present analyses were obtained from 329 children. The study group consisted of 161 (48.9%) girls and 168 (51.1%) boys, at the baseline mean (standard deviation, SD) age of the children being 7.6 (0.4) years and after 2.2 year follow-up 10.1 (0.5) years. The study protocol was approved by the Research Ethics Committee of the Hospital District of Northern Savo. All participating children and their parents gave their informed written consent. Assessment of craniofacial structures and dental occlusion Craniofacial structures and dental occlusion were clinically evaluated by a standard orthodontic screening method by an experienced orthodontist (TI). The occlusion was assessed according to the modified method of Björk et al. (21) in the intercuspal position. The recorded variables included molar occlusion (distal, normal, or mesial), overjet (mm), overbite (mm), crowding, and spacing per dental arch (≥2 mm), anterior and lateral open bite (≥2 mm) as well as crossbite and scissors bite. The shape of the palate was visually defined as wide, normal, or narrow. The existence of adipose tissue under the chin was examined by viewing the lateral profile of the child to asses if there was a visible amount of submandibular fat. The facial profile was also assessed visually (convex, normal, concave, vertical anterior facial dimension). To assess the airway space between the tonsils the children were asked to breathe through their nose, which relaxes the pharynx and palatal area. The tonsils were considered hypertrophied, if there was a space of 1 cm or less between the tonsils in visual inspection. The definition corresponds to Classes 3–4 described by Brodsky (22). Soft palatal morphology was classified using a clinical examination on maximal mouth opening and tongue protrusion in the seated position, as described by Mallampati et al. (23). With Mallampati Classes I and II, the morphology was classified as vertically normal/large throat and with Classes III and IV as vertically restricted throat. Dominance of mouth breathing was assessed visually during the clinical examination. Previous or ongoing orthodontic treatment was checked from dental recordings and classified according to the most prevalent treatment modalities in Finnish children among the studied age groups: Quad helix, head gear, or other (mostly eruption guidance appliance). Noteworthy, if an examination showed treatment need, a child was referred to an appropriate professional (i.e., dentist, orthodontist, physician). Assessment of body composition Body fat percentage was measured the children having voided, being in light clothing and in supine position, and after removing all metal objects using the Lunar Prodigy Advance® dual-energy X-ray absorptiometry device (GE Medical Systems, Madison, Wisconsin, USA). Assessment of sleep, SDB, and associated factors The questions in our sleep questionnaire were based on an established questionnaire that has been used to screen for sleep disturbances and SDB (24) and modified in the present study for the parents to fill out on behalf of their children. The parents were asked to answer to questions regarding the quantity and quality of sleep, symptoms of SDB, upper airway infections, adenotonsillectomy, and other operative treatments. SDB symptom was defined as witnessed breathing pauses (apneas) (sometimes, usually, or always/almost always) and/or frequent (most of the sleeping time or frequently) and/or loud (quite loudly, loudly, or extremely loudly) snoring and/or nocturnal mouth breathing (usually or always/almost always) observed by the parents. In other words, if the child had one or more of above-mentioned symptoms, he/she was defined as having SDB. Statistical methods The Chi-square statistics or the Fisher’s Exact Test was used to compare the prevalence of abnormal craniofacial structures and dental malocclusions between children with SDB and those without it. The Student’s t-test was used to compare body fat percentage between girls and boys and between children with SDB and those without it. Multiple logistic regression analysis using a stepwise entering selection procedure was used to study the associations of craniofacial abnormalities (no versus yes), dental malocclusions (no versus yes), mouth breathing (no versus yes), malocclusion in orthodontic treatment (no versus yes), and body fat percentage (per 1 standard deviation increase) at the age of 6–8 years with the risk of having or developing SDB on average 2.2 years later after adjustment for sex. Associations with P values of <0.05 were considered statistically significant. All statistical analyses were performed using the IBM SPSS Statistics®, Version 21 (IBM Corp., Armonk, New York, USA). Results Characteristics of children The mean (standard deviation, SD) body fat percentage at the age of 6–8 years was 22.3 (7.9) among girls and 17.6 (8.0) among boys (P < 0.001 for difference) and at the age of 9–11 25.2 (8.6) and 21.7 (9.5), respectively (P = 0.001). Of all 329 children, 33 (10.8%) had SDB at baseline and 38 (11.6%) had SDB at 2-year follow-up. SDB disappeared in 16 (4.8%) children during 2-year follow-up. It appeared in 21 (7.1%) out of 296 children without SDB at baseline during 2-year follow-up. At baseline, children with SDB were more likely to have convex facial profile, increased lower facial height, mandibular retrusion, tonsillar hypertrophy, and mouth breathing than those without SDB (Table 1). At 2-year follow-up, children with SDB were more likely to have convex facial profile, mandibular retrusion, and mouth breathing than those without it (Table 1). Table 1. Characteristics of children with SDB and those without it at baseline and at 2.2-year follow-up. Children examined at baseline (n = 329) Children examined at 2.2-year follow-up (n = 329) Children with SDB (n = 33) Children without SDB (n = 296) P value Children with SDB (n = 38) Children without SDB (n = 291) P value Distal molar occlusion 12 (36.4) 87 (29.4) 0.408 13 (34.2) 68 (23.4) 0.145 Crossbite 7 (21.2) 35 (11.8) 0.163a 5 (13.2) 24 (8.2) 0.356a Open bite 3 (9.4) 9 (3.0) 0.101a 0 (0) 3 (1.0) 1.000a Crowding 16 (48.5) 151 (51.0) 0.783 13 (34.2) 127 (43.6) 0.269 Scissors bite 1 (3.0) 3 (1.0) 0.346a 3 (7.9) 8 (2.7) 0.122a Convex facial profile 18 (54.5) 93 (31.4) 0.008 20 104 (35.7) 0.043 Increased lower facial height 12 (36.4) 59 (19.9) 0.030 (52.6)12 (31.6) 58 (19.9) 0.099 Mandibular retrusion 16 (48.5) 82 (27.7) 0.013 20 (52.6) 93 (32.0) 0.012 Maxillary retrusion 0 (0) 6 (2.0) 1.000a 3 (7.9) 6 (2.1) 0.073a Decreased palatal width 7 (21.2) 34 (11.5) 0.158a 8 (21.1) 31 (10.7) 0.103a Tonsillar hypertrophy 8 (24.2) 22 (7.4) 0.005a 6 (15.8) 19 (6.5) 0.053a Vertically restricted throatb 17 (51.5) 130 (43.9) 0.405 10 (26.3) 90 (30.9) 0.561 Mouth breathing 9 (27.3) 18 (6.1) <0.001a 7 (18.4) 12 (4.1) 0.003a Malocclusion in orthodontic treatment 3 (9.1) 22 (7.4) 0.727a 10 (26.3) 52 (17.9) 0.211 Thick neck 3 (9.1) 44 (14.9) 0.598a 1 (2.6) 4 (1.4) 0.461a Adipose tissue under the chin 9 (27.3) 96 (33.4) 0.474 11 (28.9) 47 (16.3) 0.056 Fat percentagec 19.2 (8.6) 20.0 (8.2) 0.608c 25.5 (10.1) 23.1 (9.1) 0.135c Children examined at baseline (n = 329) Children examined at 2.2-year follow-up (n = 329) Children with SDB (n = 33) Children without SDB (n = 296) P value Children with SDB (n = 38) Children without SDB (n = 291) P value Distal molar occlusion 12 (36.4) 87 (29.4) 0.408 13 (34.2) 68 (23.4) 0.145 Crossbite 7 (21.2) 35 (11.8) 0.163a 5 (13.2) 24 (8.2) 0.356a Open bite 3 (9.4) 9 (3.0) 0.101a 0 (0) 3 (1.0) 1.000a Crowding 16 (48.5) 151 (51.0) 0.783 13 (34.2) 127 (43.6) 0.269 Scissors bite 1 (3.0) 3 (1.0) 0.346a 3 (7.9) 8 (2.7) 0.122a Convex facial profile 18 (54.5) 93 (31.4) 0.008 20 104 (35.7) 0.043 Increased lower facial height 12 (36.4) 59 (19.9) 0.030 (52.6)12 (31.6) 58 (19.9) 0.099 Mandibular retrusion 16 (48.5) 82 (27.7) 0.013 20 (52.6) 93 (32.0) 0.012 Maxillary retrusion 0 (0) 6 (2.0) 1.000a 3 (7.9) 6 (2.1) 0.073a Decreased palatal width 7 (21.2) 34 (11.5) 0.158a 8 (21.1) 31 (10.7) 0.103a Tonsillar hypertrophy 8 (24.2) 22 (7.4) 0.005a 6 (15.8) 19 (6.5) 0.053a Vertically restricted throatb 17 (51.5) 130 (43.9) 0.405 10 (26.3) 90 (30.9) 0.561 Mouth breathing 9 (27.3) 18 (6.1) <0.001a 7 (18.4) 12 (4.1) 0.003a Malocclusion in orthodontic treatment 3 (9.1) 22 (7.4) 0.727a 10 (26.3) 52 (17.9) 0.211 Thick neck 3 (9.1) 44 (14.9) 0.598a 1 (2.6) 4 (1.4) 0.461a Adipose tissue under the chin 9 (27.3) 96 (33.4) 0.474 11 (28.9) 47 (16.3) 0.056 Fat percentagec 19.2 (8.6) 20.0 (8.2) 0.608c 25.5 (10.1) 23.1 (9.1) 0.135c Data are numbers (percentages) and P-values are from Chi-square test. aP values from Fisher’s exact test. bDefined as Classes III or IV as described by Mallampati et al. (22). cData are means (standard deviations) and P values are from Student’s t-test. View Large Table 1. Characteristics of children with SDB and those without it at baseline and at 2.2-year follow-up. Children examined at baseline (n = 329) Children examined at 2.2-year follow-up (n = 329) Children with SDB (n = 33) Children without SDB (n = 296) P value Children with SDB (n = 38) Children without SDB (n = 291) P value Distal molar occlusion 12 (36.4) 87 (29.4) 0.408 13 (34.2) 68 (23.4) 0.145 Crossbite 7 (21.2) 35 (11.8) 0.163a 5 (13.2) 24 (8.2) 0.356a Open bite 3 (9.4) 9 (3.0) 0.101a 0 (0) 3 (1.0) 1.000a Crowding 16 (48.5) 151 (51.0) 0.783 13 (34.2) 127 (43.6) 0.269 Scissors bite 1 (3.0) 3 (1.0) 0.346a 3 (7.9) 8 (2.7) 0.122a Convex facial profile 18 (54.5) 93 (31.4) 0.008 20 104 (35.7) 0.043 Increased lower facial height 12 (36.4) 59 (19.9) 0.030 (52.6)12 (31.6) 58 (19.9) 0.099 Mandibular retrusion 16 (48.5) 82 (27.7) 0.013 20 (52.6) 93 (32.0) 0.012 Maxillary retrusion 0 (0) 6 (2.0) 1.000a 3 (7.9) 6 (2.1) 0.073a Decreased palatal width 7 (21.2) 34 (11.5) 0.158a 8 (21.1) 31 (10.7) 0.103a Tonsillar hypertrophy 8 (24.2) 22 (7.4) 0.005a 6 (15.8) 19 (6.5) 0.053a Vertically restricted throatb 17 (51.5) 130 (43.9) 0.405 10 (26.3) 90 (30.9) 0.561 Mouth breathing 9 (27.3) 18 (6.1) <0.001a 7 (18.4) 12 (4.1) 0.003a Malocclusion in orthodontic treatment 3 (9.1) 22 (7.4) 0.727a 10 (26.3) 52 (17.9) 0.211 Thick neck 3 (9.1) 44 (14.9) 0.598a 1 (2.6) 4 (1.4) 0.461a Adipose tissue under the chin 9 (27.3) 96 (33.4) 0.474 11 (28.9) 47 (16.3) 0.056 Fat percentagec 19.2 (8.6) 20.0 (8.2) 0.608c 25.5 (10.1) 23.1 (9.1) 0.135c Children examined at baseline (n = 329) Children examined at 2.2-year follow-up (n = 329) Children with SDB (n = 33) Children without SDB (n = 296) P value Children with SDB (n = 38) Children without SDB (n = 291) P value Distal molar occlusion 12 (36.4) 87 (29.4) 0.408 13 (34.2) 68 (23.4) 0.145 Crossbite 7 (21.2) 35 (11.8) 0.163a 5 (13.2) 24 (8.2) 0.356a Open bite 3 (9.4) 9 (3.0) 0.101a 0 (0) 3 (1.0) 1.000a Crowding 16 (48.5) 151 (51.0) 0.783 13 (34.2) 127 (43.6) 0.269 Scissors bite 1 (3.0) 3 (1.0) 0.346a 3 (7.9) 8 (2.7) 0.122a Convex facial profile 18 (54.5) 93 (31.4) 0.008 20 104 (35.7) 0.043 Increased lower facial height 12 (36.4) 59 (19.9) 0.030 (52.6)12 (31.6) 58 (19.9) 0.099 Mandibular retrusion 16 (48.5) 82 (27.7) 0.013 20 (52.6) 93 (32.0) 0.012 Maxillary retrusion 0 (0) 6 (2.0) 1.000a 3 (7.9) 6 (2.1) 0.073a Decreased palatal width 7 (21.2) 34 (11.5) 0.158a 8 (21.1) 31 (10.7) 0.103a Tonsillar hypertrophy 8 (24.2) 22 (7.4) 0.005a 6 (15.8) 19 (6.5) 0.053a Vertically restricted throatb 17 (51.5) 130 (43.9) 0.405 10 (26.3) 90 (30.9) 0.561 Mouth breathing 9 (27.3) 18 (6.1) <0.001a 7 (18.4) 12 (4.1) 0.003a Malocclusion in orthodontic treatment 3 (9.1) 22 (7.4) 0.727a 10 (26.3) 52 (17.9) 0.211 Thick neck 3 (9.1) 44 (14.9) 0.598a 1 (2.6) 4 (1.4) 0.461a Adipose tissue under the chin 9 (27.3) 96 (33.4) 0.474 11 (28.9) 47 (16.3) 0.056 Fat percentagec 19.2 (8.6) 20.0 (8.2) 0.608c 25.5 (10.1) 23.1 (9.1) 0.135c Data are numbers (percentages) and P-values are from Chi-square test. aP values from Fisher’s exact test. bDefined as Classes III or IV as described by Mallampati et al. (22). cData are means (standard deviations) and P values are from Student’s t-test. View Large Risk factors for SDB Male gender, distal molar occlusion, mouth breathing, and increased body fat percentage at baseline were associated with increased risk of having SDB at 2.2-year follow-up (Table 2). Mouth breathing was the strongest baseline predictor of SDB at 2.2-year follow-up. Children with mouth breathing at baseline had a 4.4-times higher risk of SDB at 2.2-year follow-up than those without it. Table 2. Baseline predictors for having SDB at 2.2-year follow-up among all 329 children. Odds ratio 95% confidence interval P value Male gender 2.2 1.0–4.6 0.042 Distal molar occlusion 2.2 1.1–4.6 0.032 Mouth breathing 4.4 1.7–11.4 0.002 1 SD increase in body fat percentage 1.5 1.1–2.1 0.015 Odds ratio 95% confidence interval P value Male gender 2.2 1.0–4.6 0.042 Distal molar occlusion 2.2 1.1–4.6 0.032 Mouth breathing 4.4 1.7–11.4 0.002 1 SD increase in body fat percentage 1.5 1.1–2.1 0.015 Data are from stepwise logistic regression models, the effect of gender was considered in each step. Only statistically significant determinants are given. View Large Table 2. Baseline predictors for having SDB at 2.2-year follow-up among all 329 children. Odds ratio 95% confidence interval P value Male gender 2.2 1.0–4.6 0.042 Distal molar occlusion 2.2 1.1–4.6 0.032 Mouth breathing 4.4 1.7–11.4 0.002 1 SD increase in body fat percentage 1.5 1.1–2.1 0.015 Odds ratio 95% confidence interval P value Male gender 2.2 1.0–4.6 0.042 Distal molar occlusion 2.2 1.1–4.6 0.032 Mouth breathing 4.4 1.7–11.4 0.002 1 SD increase in body fat percentage 1.5 1.1–2.1 0.015 Data are from stepwise logistic regression models, the effect of gender was considered in each step. Only statistically significant determinants are given. View Large Mandibular retrusion, a vertically large or normal throat, adipose tissue under the chin and malocclusion in orthodontic treatment at baseline were associated with increased risk of developing SDB during 2.2-year follow-up (Table 3). Malocclusion in orthodontic treatment was the strongest baseline predictor of developing SBD during 2.2-year follow-up. Children who had a malocclusion in orthodontic treatment at baseline had a 5.0 times higher risk of SBD than those without it. Table 3. Baseline predictors for incident SBD at 2.2-year follow-up among 296 children who had no SDB at baseline. Odds ratio 95% confidence interval P value Mandibular retrusion 3.4 1.3–8.9 0.012 Vertically restricted throata 0.2 0.1–0.7 0.011 Adipose tissue under the chin 2.8 1.1–7.2 0.034 Malocclusion in orthodontic treatment 5.0 1.3–18.4 0.016 Odds ratio 95% confidence interval P value Mandibular retrusion 3.4 1.3–8.9 0.012 Vertically restricted throata 0.2 0.1–0.7 0.011 Adipose tissue under the chin 2.8 1.1–7.2 0.034 Malocclusion in orthodontic treatment 5.0 1.3–18.4 0.016 Data are from stepwise logistic regression models, the effect of gender was considered in each step. Only statistically significant determinants are given. aDefined as Classes III or IV as described by Mallampati et al. (22). View Large Table 3. Baseline predictors for incident SBD at 2.2-year follow-up among 296 children who had no SDB at baseline. Odds ratio 95% confidence interval P value Mandibular retrusion 3.4 1.3–8.9 0.012 Vertically restricted throata 0.2 0.1–0.7 0.011 Adipose tissue under the chin 2.8 1.1–7.2 0.034 Malocclusion in orthodontic treatment 5.0 1.3–18.4 0.016 Odds ratio 95% confidence interval P value Mandibular retrusion 3.4 1.3–8.9 0.012 Vertically restricted throata 0.2 0.1–0.7 0.011 Adipose tissue under the chin 2.8 1.1–7.2 0.034 Malocclusion in orthodontic treatment 5.0 1.3–18.4 0.016 Data are from stepwise logistic regression models, the effect of gender was considered in each step. Only statistically significant determinants are given. aDefined as Classes III or IV as described by Mallampati et al. (22). View Large Discussion The present longitudinal study showed that already at the age of 6–8 years there are certain morphological and functional features that can predict developing SDB at the age of 9–11 years. Especially higher body adiposity and mouth breathing, as well as distal molar occlusion seemed to predispose to the development of SDB already in childhood. Furthermore, as in adults (25), male gender also increased the risk of SDB. Adipose tissue under the chin, mandibular retrusion, vertically normal/large throat, and malocclusion in orthodontic treatment were associated with developing SDB during the 2.2 year follow-up. Adenotonsillar hypertrophy is the most common risk factor for pediatric SDB (10, 14). The volume of the adenoid and tonsils increases from birth to the age of 12 years, the peak of their size proportional to the skeletal structures being at the age of 5–6 years (10). Even though nasal resistance decreases from 9 to 13 years of age, there is a transient prepubertal increase in the resistance, a phenomenon suggested to result from hormonal changes (26). According to Papaioannou et al. (27), during the first 8 years of life the pharyngeal lymphoid tissue is likely to be exposed to external microbial stimuli that promote cellular proliferation. In line, pediatric SDB is most common in pre-school and early school years (28). We found that tonsillar hypertrophy was common among children with SDB and that mouth breathing, usually co-existing with tonsillar hypertrophy, at the age of 6–8 years was associated with increased risk of SDB 2.2 years later. Interestingly, children with vertically large or normal throat had increased risk for SDB. The same children also tended to have hypertrophied tonsils more often than those with vertically restricted throat. This may indicate that those children had developed a lowered position of the tongue to improve their breathing, which is in line with the results of the classical study of Linder-Aronson (29). Further, Suri et al. showed that abnormal palatal morphology significantly predicted a poor outcome of the treatment of SDB with adenotonsillectomy and suggested that a delay in treating the hypertrophied adenoid and tonsils may promote abnormal craniofacial growth, leading to residual SDB (30). Malocclusion in orthodontic treatment at baseline was associated with increased risk of developing SDB during 2.2-year follow-up in our study. As found in previous studies deviant craniofacial morphology, such as retrognathic mandible, reduced width of maxillary dental arch, and anterior open bite are associated with SDB among children (31–33). In our study, children with SDB were more likely to have facial convexity, mandibular retrusion and increased facial height than those without it. Furthermore, distal molar occlusion at the age of 6–8 years predicted SDB 2.2 years later. These malocclusions are usually diagnosed and early orthodontic treatment is initiated at that age in Finland. The impact of different treatment modalities would require further examination since, basically, early orthodontic treatment is thought to prevent SDB in adulthood by modifying the deviant craniofacial morphology (17, 18). Adiposity has been observed to be an important risk factor for developing SDB in children (13, 25). A recent study showed that especially increased amount of visceral fat was associated with more serious manifestations of SDB in a population sample of children (34). Parallel to the results of these studies, we found that a higher body fat percentage at the age of 6–8 years was associated with a higher risk of having SBD 2.2 years later and further, adipose tissue under the chin was associated with increased risk of developing SDB during 2.2-year follow-up. The mechanism by which adiposity predisposes to SDB may be the mass loading of upper airway and respiratory muscles (5) causing alterations to the structure and function of these muscles, the reduction of chest wall compliance, changes in respiratory drive and the impairment of functional residual capacity, all of which increase the risk of upper airway obstruction (25). It is alarming that overweight and obesity are becoming more common in children and adolescents in many developed countries (35). In Finland, 10% of children and 26% of adolescents have been found to be overweight (36). In fact, obese children have been observed to have an increased risk of persistent SDB even after adenotonsillectomy, which is the first line treatment for pediatric SDB (25). In children, the associations of overweight and obesity with SDB may not be straightforward, and the relationship may be modified by other factors, such as age, ethnicity, and craniofacial morphology (25). Generally, sleep disorders are suggested to be more prevalent in boys (37) and like in adults, boys to have more SDB compared with girls (38). There are also studies to show no gender difference in the prevalence of SDB (39, 40). Further, some questionnaire-based studies show boys to have more SDB compared with girls (38, 41). The present study showed male gender to increase the risk of SDB. A strength of our study is that we used a population-based sample of children to study the longitudinal associations of body fat percentage, dental malocclusions, other craniofacial abnormalities, mouth breathing, and orthodontic treatment with SDB. We assessed body fat percentage using DXA that is a reliable and valid measure of body fat content (20). Limitations Because of the epidemiological nature of the study we could not conduct demanding polysomnographic examinations to define sleep disturbances. Instead, we used a questionnaire filled out by the parents to assess SDB symptoms. Some parents may have been unaware of their children’s sleeping pattern that may have caused inaccuracy in reporting. However, our sleep questionnaire was based on an established Finnish questionnaire (24) that is a widely used method to assess SDB (42). After follow-up we had complete data of 64% of the children studied at baseline. The burden of numerous medical, nutritional, physical, psychological, and dental examinations may have caused the quite large proportion of drop-outs. We did not examine the size of the adenoids, because in this age group the only ethical and reliable method would have been magnetic resonance imaging that was not feasible because of the epidemiological nature of the study. However, as the hypertrophy of the adenoid and tonsils typically coexist and indicate the amount of lymphoid tissue in the pharynx, it may not be relevant to consider them as different conditions. Further, we did not have the opportunity for a rhinomanometric examination to examine nasal resistance and the size of the nasopharyngeal area. Finally, the observational design of our study makes it difficult to draw conclusions about causal relationships between the exposure and outcome variables and given the large confidence intervals, the study results need to be interpreted with caution. Conclusions Deviant craniofacial morphology, mouth breathing, adiposity, and male gender may predict SDB in childhood. These findings are useful in identifying growing children at increased risk of developing SDB. Children with these features could be candidates for early intervention to prevent the progression of SDB later in life. Funding The PANIC Study has been financially supported by grants from the Ministry of Social Affairs and Health of Finland (090/KTL/TE/2008; 148/KTL/TE/2009; 178/THL/TE/2010; 178/THL/TE/2011), the Ministry of Education and Culture of Finland (105/627/2006; 104/626/2008; 121/627/2009; 108/627/2010; 55/627/2011; OKM/48/626/2013), the University of Eastern Finland, the Finnish Innovation Fund Sitra (5451031/1), the Social Insurance Institution of Finland (22/26/2008), the Finnish Cultural Foundation (00090566; 00100516), the Juho Vainio Foundation, the Foundation for Pediatric Research, the Paulo Foundation, the Paavo Nurmi Foundation, the Diabetes Research Foundation, and the Kuopio University Hospital (EVO 5031343), the Yrjö Jahnsson Foundation (66779), Jenny and Antti Wihuri Foundation and Päivikki and Sakari Sohlberg Foundation. Conflict of Interest None to declare. References 1. Li , H.Y. and Lee , L.A . ( 2009 ) Sleep-disordered breathing in children . Chang Gung Medical Journal , 32 , 247 – 257 . Google Scholar PubMed 2. Bradley , T.D. and Floras , J.S . ( 2009 ) Obstructive sleep apnoea and its cardiovascular consequences . Lancet (London, England) , 373 , 82 – 93 . Google Scholar CrossRef Search ADS PubMed 3. Young , T. , Palta , M. , Dempsey , J. , Skatrud , J. , Weber , S. and Badr , S . ( 1993 ) The occurrence of sleep-disordered breathing among middle-aged adults . The New England Journal of Medicine , 328 , 1230 – 1235 . Google Scholar CrossRef Search ADS PubMed 4. Ng , D.K. , Lam , Y.Y. , Kwok , K.L. and Chow , P.Y . ( 2004 ) Obstructive sleep apnoea syndrome and obesity in children . Hong Kong Medical Journal , 10 , 44 – 48 . Google Scholar PubMed 5. Ng , D.K. , Chow , P.Y. , Chan , C.H. , Kwok , K.L. , Cheung , J.M. and Kong , F.Y . ( 2006 ) An update on childhood snoring . Acta Paediatrica (Oslo, Norway: 1992) , 95 , 1029 – 1035 . Google Scholar CrossRef Search ADS PubMed 6. Hultcrantz , E. and Löfstrand Tideström , B . ( 2009 ) The development of sleep disordered breathing from 4 to 12 years and dental arch morphology . International Journal of Pediatric Otorhinolaryngology , 73 , 1234 – 1241 . Google Scholar CrossRef Search ADS PubMed 7. Ali , N.J. , Pitson , D.J. and Stradling , J.R . ( 1993 ) Snoring, sleep disturbance, and behaviour in 4-5 year olds . Archives of Disease in Childhood , 68 , 360 – 366 . Google Scholar CrossRef Search ADS PubMed 8. Ali , N.J. , Pitson , D. and Stradling , J.R . ( 1994 ) Natural history of snoring and related behaviour problems between the ages of 4 and 7 years . Archives of Disease in Childhood , 71 , 74 – 76 . Google Scholar CrossRef Search ADS PubMed 9. Ikävalko , T. et al. ( 2012 ) Craniofacial morphology but not excess body fat is associated with risk of having sleep-disordered breathing–the PANIC Study (a questionnaire-based inquiry in 6-8-year-olds) . European Journal of Pediatrics , 171 , 1747 – 1752 . Google Scholar CrossRef Search ADS PubMed 10. Dayyat , E. , Kheirandish-Gozal , L. , Gozal , D . ( 2007 ) Childhood obstructive sleep apnea: one or two distinct disease entities ? Sleep Medicine Clinics , 2 , 433 – 444 . Google Scholar CrossRef Search ADS PubMed 11. Leinum , C.J. , Dopp , J.M. and Morgan , B.J . ( 2009 ) Sleep-disordered breathing and obesity: pathophysiology, complications, and treatment . Nutrition in Clinical Practice , 24 , 675 – 687 . Google Scholar CrossRef Search ADS PubMed 12. Marcus , C.L. , Curtis , S. , Koerner , C.B. , Joffe , A. , Serwint , J.R. and Loughlin , G.M . ( 1996 ) Evaluation of pulmonary function and polysomnography in obese children and adolescents . Pediatric Pulmonology , 21 , 176 – 183 . Google Scholar CrossRef Search ADS PubMed 13. Verhulst , S.L. , Van Gaal , L. , De Backer , W. and Desager , K . ( 2008 ) The prevalence, anatomical correlates and treatment of sleep-disordered breathing in obese children and adolescents . Sleep Medicine Reviews , 12 , 339 – 346 . Google Scholar CrossRef Search ADS PubMed 14. Arens , R. et al. ( 2003 ) Upper airway size analysis by magnetic resonance imaging of children with obstructive sleep apnea syndrome . American Journal of Respiratory and Critical Care Medicine , 167 , 65 – 70 . Google Scholar CrossRef Search ADS PubMed 15. Flores-Mir , C. , Korayem , M. , Heo , G. , Witmans , M. , Major , M.P. and Major , P.W . ( 2013 ) Craniofacial morphological characteristics in children with obstructive sleep apnea syndrome: a systematic review and meta-analysis . Journal of the American Dental Association (1939) , 144 , 269 – 277 . Google Scholar CrossRef Search ADS PubMed 16. Guilleminault , C. and Li , K.K . ( 2004 ) Maxillomandibular expansion for the treatment of sleep-disordered breathing: preliminary result . The Laryngoscope , 114 , 893 – 896 . Google Scholar CrossRef Search ADS PubMed 17. Ashok , N. , Varma , N.K. , Ajith , V.V. and Gopinath , S . ( 2014 ) Effect of rapid maxillary expansion on sleep characteristics in children . Contemporary Clinical Dentistry , 5 , 489 – 494 . Google Scholar CrossRef Search ADS PubMed 18. Hänggi , M.P. , Teuscher , U.M. , Roos , M. and Peltomäki , T.A . ( 2008 ) Long-term changes in pharyngeal airway dimensions following activator-headgear and fixed appliance treatment . European Journal of Orthodontics , 30 , 598 – 605 . Google Scholar CrossRef Search ADS PubMed 19. Villa , M.P. , Miano , S. and Rizzoli , A . ( 2012 ) Mandibular advancement devices are an alternative and valid treatment for pediatric obstructive sleep apnea syndrome . Sleep & Breathing , 16 , 971 – 976 . Google Scholar CrossRef Search ADS 20. Eloranta , A.M. et al. ( 2012 ) Dietary factors associated with overweight and body adiposity in Finnish children aged 6-8 years: the PANIC Study . International Journal of Obesity (2005) , 36 , 950 – 955 . Google Scholar CrossRef Search ADS PubMed 21. Björk , A. , Krebs , B. and Solow , B . ( 1964 ) A method for epidemiological registration of malocclusion . Acta Odontologica Scandinavica , 22 , 27 – 41 . Google Scholar CrossRef Search ADS PubMed 22. Brodsky , L . ( 1989 ) Modern assessment of tonsils and adenoids . Pediatric Clinics of North America , 36 , 1551 – 1569 . Google Scholar CrossRef Search ADS PubMed 23. Mallampati , S.R. et al. 1985 A clinical sign to predict difficult tracheal intubation: a prospective study . Canadian Anaesthetists’ Society Journal , 32 , 429 – 434 . Google Scholar CrossRef Search ADS PubMed 24. Partinen , M. and Gislason , T . ( 1995 ) Basic Nordic Sleep Questionnaire (BNSQ): a quantitated measure of subjective sleep complaints . Journal of Sleep Research , 4 , 150 – 155 . Google Scholar CrossRef Search ADS PubMed 25. Kohler , M.J. and van den Heuvel C.J . ( 2008 ) Is there a clear link between overweight/obesity and sleep disordered breathing in children ? Sleep Medicine Reviews , 12 , 347 – 361 . Google Scholar CrossRef Search ADS PubMed 26. Crouse , U. , Laine-Alava , M.T. and Warren , D.W . ( 2000 ) Nasal impairment in prepubertal children . American Journal of Orthodontics and Dentofacial Orthopedics , 118 , 69 – 74 . Google Scholar CrossRef Search ADS PubMed 27. Papaioannou , G. , Kambas , I. , Tsaoussoglou , M. , Panaghiotopoulou-Gartagani , P. , Chrousos , G. and Kaditis A.G . ( 2013 ) Age-dependent changes in the size of adenotonsillar tissue in childhood: implications for sleep-disordered breathing . The Journal of Pediatrics , 162 , 269 – 74.e4 . Google Scholar CrossRef Search ADS PubMed 28. Corbo , G. M. et al. ( 2001 ) Snoring in 9- to 15-year-old children: risk factors and clinical relevance . Pediatrics , 108 , 1149 – 1154 . Google Scholar CrossRef Search ADS PubMed 29. Linder-Aronson , S . ( 1970 ) Adenoids. Their effect on mode of breathing and nasal airflow and their relationship to characteristics of the facial skeleton and the denition. A biometric, rhino-manometric and cephalometro-radiographic study on children with and without adenoids . Acta Otolaryngologica , 265 , 1 – 132 . 30. Suri , J.C. , Sen , M.K. , Venkatachalam , V.P. , Bhool , S. , Sharma , R. , Elias , M. and Adhikari , T . ( 2015 ) Outcome of adenotonsillectomy for children with sleep apnea . Sleep Medicine , 16 , 1181 – 1186 . Google Scholar CrossRef Search ADS PubMed 31. Löfstrand-Tideström , B , Thilander , B , Ahlqvist-Rastad , J. , Jakobsson , O. and Hultcrantz , E . ( 1999 ) Breathing obstruction in relation to craniofacial and dental arch morphology in 4-year-old children . European Journal of Orthodontics , 21 , 323 – 332 . Google Scholar CrossRef Search ADS PubMed 32. Marino , A. , Malagnino , I. , Ranieri , R. , Villa , M.P. and Malagola , C . ( 2009 ) Craniofacial morphology in preschool children with obstructive sleep apnoea syndrome . European Journal of Paediatric Dentistry , 10 , 181 – 184 . Google Scholar PubMed 33. Pirilä-Parkkinen , K. , Pirttiniemi , P. , Nieminen , P. , Tolonen , U. , Pelttari , U. and Löppönen , H . ( 2009 ) Dental arch morphology in children with sleep-disordered breathing . European Journal of Orthodontics , 31 , 160 – 167 . Google Scholar CrossRef Search ADS PubMed 34. Bixler , E.O. et al. ( 2016 ) Natural history of sleep disordered breathing in prepubertal children transitioning to adolescence . The European Respiratory Journal , 47 , 1402 – 1409 . Google Scholar CrossRef Search ADS PubMed 35. Kipping , R.R. , Jago , R. and Lawlor , D.A . ( 2008 ) Obesity in children. Part 1: Epidemiology, measurement, risk factors, and screening . BMJ (Clinical research ed.) , 337 , a1824 . Google Scholar CrossRef Search ADS PubMed 36. Vuorela , N. , Saha , M.T. and Salo , M . ( 2009 ) Prevalence of overweight and obesity in 5- and 12-year-old Finnish children in 1986 and 2006 . Acta Paediatrica (Oslo, Norway: 1992) , 98 , 507 – 512 . Google Scholar CrossRef Search ADS PubMed 37. Paavonen , E.J. et al. ( 2000 ) Sleep problems of school-aged children: a complementary view . Acta Paediatrica (Oslo, Norway: 1992) , 89 , 223 – 228 . Google Scholar CrossRef Search ADS PubMed 38. Gill , A.I. , Schaughency , E. and Galland , B.C . ( 2012 ) Prevalence and factors associated with snoring in 3-year olds: early links with behavioral adjustment . Sleep Medicine , 13 , 1191 – 1197 . Google Scholar CrossRef Search ADS PubMed 39. Goodwin , J.L. et al. ; Tucson Children’s Assessment of Sleep Apnea Study . 2003 Symptoms related to sleep-disordered breathing in white and Hispanic children: the Tucson Children’s Assessment of Sleep Apnea Study . Chest , 124 , 196 – 203 . Google Scholar CrossRef Search ADS PubMed 40. Liukkonen , K. , Virkkula , P. , Aronen , E.T. , Kirjavainen , T. and Pitkäranta , A . ( 2008 ) All snoring is not adenoids in young children . International Journal of Pediatric Otorhinolaryngology , 72 , 879 – 884 . Google Scholar CrossRef Search ADS PubMed 41. Ersu , R. et al. ( 2004 ) Prevalence of snoring and symptoms of sleep-disordered breathing in primary school children in Istanbul . Chest , 126 , 19 – 24 . Google Scholar CrossRef Search ADS PubMed 42. Kapuniai , L.E. , Andrew , D.J. , Crowell , D.H. and Pearce , J.W . ( 1988 ) Identifying sleep apnea from self-reports . Sleep , 11 , 430 – 436 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2017. Published by Oxford University Press on behalf of the European Orthodontic Society. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

Journal

The European Journal of OrthodonticsOxford University Press

Published: Jul 11, 2017

There are no references for this article.

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off