European Journal of Pediatrics

, Volume 171, Issue 12, pp 1747–1752

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)

  • Tiina Ikävalko
  • Henri Tuomilehto
  • Riitta Pahkala
  • Tuomo Tompuri
  • Tomi Laitinen
  • Riitta Myllykangas
  • Anu Vierola
  • Virpi Lindi
  • Matti Närhi
  • Timo A. Lakka
Leading Article

DOI: 10.1007/s00431-012-1757-x

Cite this article as:
Ikävalko, T., Tuomilehto, H., Pahkala, R. et al. Eur J Pediatr (2012) 171: 1747. doi:10.1007/s00431-012-1757-x

Abstract

We investigated the associations of dental occlusion, other craniofacial features and body fat with paediatric sleep-disordered breathing (SDB) in a representative population sample of 491 Finnish children 6–8 years of age. Overweight and obesity were defined using age- and sex-specific body mass index cutoffs by International Obesity Task Force (IOTF) criteria. Body fat percentage was assessed by dual-energy X-ray absorptiometry. Facial proportions, dental occlusion and soft tissue structures were evaluated by an orthodontist. Sleep was assessed by a sleep questionnaire administered by the parents. SDB was defined as apnoeas, frequent or loud snoring or nocturnal mouth breathing observed by the parents. The prevalence of SDB was 9.9 % with no difference between boys and girls. The median (interquartile range) of body fat percentage was 20.6 (17.4–27.1) in girls and 15.0 (11.4–21.6) in boys. Altogether 11.4 % of boys and 15.6 % of girls were classified as having overweight or obesity according to the IOTF criteria. There was no difference in the prevalence of overweight, obesity or body fat percentage between children with SDB and those without it. Children with tonsillar hypertrophy had a 3.7 times higher risk of suffering SDB than those with normal size tonsils after adjustment for age, sex and body fat percentage. Furthermore, children with cross bite had a 3.3 times higher risk of having SDB than those without cross bite, and children with a convex facial profile had a 2.6 times higher risk of having SDB than those with a normal facial profile. Conclusion: Abnormal craniofacial morphology, but not excess body fat, is associated with an increased risk of having SDB in 6–8-year-old children. A simple model of necessary clinical examinations (i.e. facial profile, dental occlusion and tonsils) is recommended to recognize children with an increased risk of SDB.

Keywords

Sleep-disordered breathing Craniofacial abnormalities Dental occlusion Tonsillar hypertrophy Overweight Obesity Childhood 

Introduction

Sleep disturbances are nowadays a public health concern throughout the world. They affect millions of people, and their prevalence is increasing not only in adults but also in children. Sleep-disordered breathing (SDB) is one of the most common sleep disturbances; it represents a continuum of symptoms from simple snoring to obstructive sleep apnoea syndrome (OSAS) [36]. While the prevalence of OSAS in adults is 2–10 % [37], the prevalence of snoring is much higher [37]. The prevalence of OSAS among children and adolescents has been reported to range between 1 and 3 % [1, 2, 22, 23] and that of snoring between 7 and 25 % [13, 22, 23].

It is alarming that overweight and obesity are becoming more common in children and adolescents in many developed countries [15]. A recent report revealed that 10 % of children and 26 % of adolescents are overweight in Finland [35]. Excess body fat is a well-recognized risk factor for SDB in adults [17], but it has also been proposed to be an important risk factor for paediatric SDB [20, 31]. In children, traditional risk factors for SDB include adenotonsillar hypertrophy, deviations in craniofacial morphology and dental occlusion [13, 18, 27]. Thus, the pathogenesis of SDB in children seems to be complex and multifactorial.

The early detection of SDB in children is important because there is a growing body of evidence which associates the detrimental health consequences of SDB with other health problems, such as daytime hyperactivity, attention deficit hyperactivity disorder-type manifestations and other behavioural and learning difficulties, enuresis, systemic low-grade inflammation, metabolic disturbances and compromised somatic growth and development [12]. However, the impact of growth and development at different ages on nocturnal breathing is not fully understood [16].

There are limited data on the relative importance of different risk factors for SDB in children because most studies on the associations of overweight and obesity with SDB have not included a clinical craniofacial examination or have had insufficient sample sizes. We therefore studied the associations of dental occlusion, other craniofacial features and body fat with the risk of having SDB, based on a questionnaire administered by the parents, in a representative population sample of children aged 6–8 years.

Methods

Study population

The present study is part of The Physical Activity and Nutrition in Children (PANIC) Study, which is an ongoing 2-year controlled exercise and diet intervention study in a representative population sample of 512 girls and boys who were 6–8 years of age and lived in the city of Kuopio in Eastern Finland during baseline examinations in 2007–2009. There are complete data on body composition, craniofacial morphology, dental occlusion and sleep for 466 (91 %) of all 512 children. The study protocol was approved by the Research Ethics Committee of the Hospital District of Northern Savo. Both children and their parents provided written informed consent.

Assessment of dental occlusion and other craniofacial features

Craniofacial morphology and dental occlusion were clinically evaluated by a standard orthodontic screening method by one orthodontist (TI). The occlusion was assessed according to the modified method of Björk et al. [6] in the intercuspal position. The recorded variables included molar occlusion (distal, normal or mesial), overjet (in millimetres), overbite (in millimetres), crowding (≥2 mm), spacing (≥2 mm), anterior and lateral open bite (≥2 mm) as well as cross and scissors bite. In cross bite, one or more lower posterior teeth are buccal to the upper counterpart(s), while in scissors bite, the whole occlusal surface of the upper posterior teeth is buccal to that of lower antagonistic teeth. The shape of the palate was visually defined as wide, normal or narrow. The existence of adipose tissue under the chin was assessed by viewing the lateral profile of the child and was considered positive, if there was a visible amount of submandibular fat. Facial profile (convexity, concavity and vertical dimension) was also assessed visually. The facial profile was also divided into five classes according to a picture determining the position of the chin (Fig. 1). To assess the actual airway between the tonsils, the children were asked to breathe through their nose, which then relaxes the pharynx and palatal area. The tonsils were considered hypertrophied, if there was 1 cm or less space between the tonsils evaluated visually by one orthodontist. The definition corresponds to classes 3–4 of the Brodsky classification [7]. Soft palatal morphology was classified according to the Mallampati et al. classification that is based on clinical examination with maximal mouth opening and tongue protrusion in the seated position [19]. Dominant mouth breathing was assessed visually during the clinical examination.
Fig. 1

Facial lateral profile divided into five classes determining the position of the chin

Assessment of body composition

Body height was measured in the Frankfurt plane without shoes by a wall-mounted stadiometer with the accuracy of 1 mm. Body weight was measured by the bioimpedance method using the Inbody 720 device (Biospace Co. Ltd., Seoul, South Korea) with the accuracy of 100 g. Both parameters were measured after an overnight fast. Body mass index (BMI) was calculated as weight (in kilograms) divided by height (in metres) squared. Z scores for height, weight and BMI were assessed with an obesity calculator that uses age- and sex-specific British growth reference data from 1990 [9]. Overweight and obesity were defined using the age- and sex-specific BMI cutoffs derived from growth curves corresponding to BMI values 25 and 30 in adults 18 years of age, published by the International Obesity Task Force [8]. Body fat percentage was assessed by the dual-energy X-ray absorptiometry (DXA) method using the Lunar device (Lunar Prodigy Advance, GE Healthcare, Madison, WI, USA) in the afternoon in the non-fasting state.

Assessment of sleep, SDB and associated factors

The questions in our sleep questionnaire were based on validated Finnish questionnaires that have been used to screen for sleep disturbances and SDB [25]. The parents filled out the questions regarding the child’s quantity and quality of sleep, symptoms of SDB and upper airway infections and previous operative treatments, such as adenotonsillectomy. SDB was defined as apnoeas, frequent or loud snoring or nocturnal mouth breathing observed by the parents.

Statistical methods

Chi-square and Student’s t test were used to compare the differences in the prevalence of dental malocclusions and other craniofacial abnormalities, the prevalence of overweight or obesity and the means of BMI Z score and body fat percentage between children with SDB and those without it and between boys and girls. Multivariate logistic regression analysis was used to investigate the associations of craniofacial abnormalities, dental malocclusions and body fat percentage with the risk of having SDB by entering all these variables as well as age and sex stepwise into the model. The associations were considered statistically significant if the p value was <0.05. All analyses were performed using the Statistical Package for Social Sciences, version 17.0 (SPSS Inc., Chicago, IL, USA).

Results

Characteristics of children

The median (interquartile range, IQR) age of the children was 7.6 (7.4–7.9) years. The children included 236 (48.2 %) girls and 255 (51.8 %) boys. The median (IQR) of BMI Z score was −0.11 (−0.79 to 0.57) in the girls and 0.01 (−0.72 to 0.83) in the boys. However, 15.6 % of the girls and 11.4 % of the boys were overweight (11.4 and 6.7 %, respectively) or obese (4.2 and 4.7 %, respectively). The median (IQR) of body fat percentage was 20.6 (17.4–27.1) in the girls and 15.0 (11.4–21.6) in the boys. The correlation between BMI Z score and body fat percentage was 0.883 in the girls (p < 0.001) and 0.872 in the boys (p < 0.001). The prevalences of dental malocclusions and other craniofacial abnormalities are presented in Table 1. Of all 466 children, 46 (9.9 %) had SDB, and there was no statistically significant difference in the prevalence between the genders. Of the children, 41 (8.8 %) snored in certain positions, 38 (8.2 %) had nocturnal mouth breathing, 23 (5.0 %) snored loudly, 9 (1.9 %) snored frequently and 3 (0.6 %) had frequent apnoeas.
Table 1

The numbers and percentages of children with dental malocclusions and other craniofacial abnormalities

 

All children (n = 491)

Girls (n = 236)

Boys (n = 255)

p valuea

Distal molar occlusion

145 (29.5)

77 (32.6)

68 (26.7)

0.148

Cross bite

73 (14.9)

33 (14.0)

40 (15.7)

0.596

Open bite

14 (2.9)

5 (2.1)

9 (3.5)

0.344

Crowding

254 (51.7)

124 (52.8)

130 (51.2)

0.726

Scissors bite

4 (0.8)

1 (0.4)

3 (1.2)

0.625

Convex facial profile

159 (32.4)

66 (28.1)

93 (36.6)

0.044

Increased lower facial height

103 (21.0)

44 (18.7)

59 (23.2)

0.222

Mandibular retrusion

139 (28.4)

58 (24.7)

81 (31.9)

0.077

Decreased palatal width

58 (11.6)

31 (13.2)

27 (10.3)

0.316

Tonsillar hypertrophy

44 (9.0)

22 (9.4)

22 (8.8)

0.819

Abnormal palatal morphologyb

211 (43.3)

100 (42.6)

111 (44.0)

0.821

Thick neck

71 (14.5)

35 (14.9)

36 (14.2)

0.739

Adipose tissue under the chin

155 (32.3)

72 (31.3)

83 (33.2)

0.657

aFrom chi-square test

bDefined as Mallampati et al. class III or IV

Risk factors for SDB

Children with SDB more likely had cross bite, a convex facial profile, hypertrophic tonsils and increased lower facial height than those without it (Table 2). There were no statistically significant differences in the prevalence of other craniofacial abnormalities between children with SDB and those without it (Table 2). Also body fat percentage [19.7 vs. 20 %, no significant (NS) difference], BMI Z score (0.01 vs. 0.05, NS difference) and the prevalence of overweight or obesity (13.0 vs. 13.4 %, NS difference) were similar in children with SDB and those without it. Children with tonsillar hypertrophy had a 3.7 times higher risk of suffering SDB than those with normal size tonsils after adjustment for age, sex and body fat percentage (Table 3). Furthermore, children with cross bite had a 3.3 times higher risk of having SDB than those without cross bite, and children with a convex facial profile had a 2.6 times higher risk of having SDB than those with a normal facial profile. Other craniofacial abnormalities or body fat percentage were not associated with the risk of having SDB.
Table 2

The numbers and percentages of children with dental malocclusions and other craniofacial abnormalities in children with SDB and those without it

 

Children with SDB (n = 46)

Children without SDB (n = 420)

p valuea

Distal molar occlusion

15 (32.6)

124 (29.5)

0.664

Cross bite

13 (28.3)

54 (12.9)

0.005

Open bite

3 (6.5)

10 (2.4)

0.097

Crowding

23 (50.0)

217 (51.9)

0.905

Scissors bite

1 (0.2)

3 (6.5)

0.308

Convex facial profile

24 (52.2)

131 (31.3)

0.004

Increased lower facial height

16 (34.8)

85 (20.3)

0.024

Mandibular retrusion

21 (45.7)

116 (27.6)

0.012

Decreased palatal width

8 (17.4)

45 (10.8)

0.182

Tonsillar hypertrophy

12 (26.1)

32 (7.7)

<0.001

Abnormal palatal morphologyb

22 (47.8)

178 (42.7)

0.504

Thick neck

5 (10.9)

62 (14.8)

0.468

Adipose tissue under the chin

16 (34.8)

133 (32.4)

0.748

aFrom chi-square test

bDefined as Mallampati et al. class III or IV

Table 3

The risk of having SDB in children with tonsillar hypertrophy, cross bite or convex facial profile as compared to children without respective craniofacial abnormalities

Statistically significant risk factors for SDBa

Relative risk

95 % confidence interval

p valuea

Tonsillar hypertrophy

3.7

1.7–8.2

0.001

Cross bite

3.3

1.5–7.1

0.003

Convex facial profile

2.6

1.4–5.1

0.004

aFrom multivariate logistic regression analysis by entering all dental malocclusions and other craniofacial abnormalities shown in Table 2 as well as body fat percentage, age and sex stepwise into the model

Discussion

The results of the present population-based study indicate that in children 6–8 years of age, tonsillar hypertrophy, cross bite and a convex facial profile, but not excess body fat, are risk factors for SDB. Interestingly, it has recently been demonstrated that deviations in craniofacial morphology are much more common in normal weight than overweight adult patients with OSAS [24]. Together these findings imply that there may be two different phenotypes of adult SDB: one related to excess fat tissue and the other to craniofacial abnormalities. According to the observations of the present study, some of the patients with SDB due to abnormal craniofacial morphology may be identified already in childhood.

Particularly in children, who are screened even less frequently than adults, SDB is believed to be underdiagnosed. Furthermore, the diagnostics of paediatric SDB are still far from clear [4]. Although some studies have indicated that the risk of SDB starts to increase only in older children [16, 34], the actual age of the development of SDB remains unclear. In line with the results of previous studies [1, 2, 3, 10, 13, 22, 23, 28, 29], we found that 10 % of children 6–8 years of age had SDB although less than 1 % suffered sleep apnoeas.

Traditionally, adenotonsillar enlargement has been regarded as the main cause, but also overweight has been considered a risk factor for developing SDB in children [16, 34]. In fact, obese children have an increased risk of persistent SDB after adenotonsillectomy [16]. Even though in our sample overweight or obese children did not have an increased risk of SDB, the importance of excess body fat should not be underestimated because obesity is the most prevalent risk factor for SDB in adults [11, 17, 32, 33]. 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 [16].

According to recent studies in Swedish, Finnish and Italian children, dental malocclusion with SDB seems to differ from dental malocclusion without SDB [18, 21, 27]. In these studies, the typical malocclusions were deviations in the sagittal, transversal and vertical dimensions, for example retrognathic mandible, reduced width of maxillary dental arch and anterior open bite. In our sample, only cross bite of all occlusal factors was associated with SDB. Furthermore, children with SDB had more likely tonsillar hypertrophy and a convex facial profile than those without it. These factors may lead to an abnormal breathing pattern, which seems to alter oral and facial muscular balance and likely affects skeletal and occlusal development in children [26].

SDB represents a continuum of manifestations from simple snoring to OSAS. The condition tends to progress from a mild SDB to a more severe OSA over a varying period of time, which may be surprisingly short in the case of weight gain and the lack of effective treatment [5, 30]. This highlights the importance of the early detection and treatment of the disease. Craniofacial and occlusal development occurs in childhood. Adult patients with SDB seem to have abnormalities in craniofacial morphology and dental occlusion similar to those found in children with sleep-related breathing disorders [18, 26]. This raises a question whether adulthood SDB could be prevented in some individuals by focusing on orthodontic treatment already in childhood.

To our knowledge, this is the first study in a population-based sample of children 6–8 years of age on the associations of dental malocclusions and other craniofacial abnormalities with SDB. We also had comprehensive and valid assessments of body composition, including DXA. However, the cross-sectional study design makes it difficult to draw conclusions about causal relationships of dental malocclusions and other craniofacial abnormalities with SDB. The findings may not be directly generalized to all ethnic and age groups, since almost all children were Caucasian and 6–8 years of age. 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. As the hypertrophy of adenoid and tonsils typically coexists and indicates the amount of lymphoid tissue in the pharynx, it may not be relevant to consider them as different conditions. We had no opportunity to conduct demanding polysomnographic examinations to define sleep disturbances because of the large study sample. Instead, we used a questionnaire administered by the parents to define SDB. Some parents may have been unaware of their child’s sleeping pattern that may have caused inaccuracy in reporting. However, our sleep questionnaire was based on validated Finnish questionnaires [25] that are adequately accurate and widely used methods to detect SDB [14]. Finally, we did not have an opportunity to analyse the associations of certain dental malocclusions and craniofacial abnormalities, such as scissors bite and open bite, with SDB because of their low prevalence and insufficient statistical power.

In conclusion, abnormal craniofacial morphology, but not excess body fat, was associated with SDB in children 6–8 years of age. If a patient suffers from symptoms of SDB, his or her craniofacial status and dental occlusion need to be examined. On the other hand, patients with dental malocclusions, deviant craniofacial features and tonsillar enlargement should always be examined as regards to their sleeping habits, snoring and pauses in breathing during sleep. Children with tonsillar hypertrophy, cross bite and convex facial profile could be candidates for early intervention and orthodontic treatment to prevent the progression of SDB in coming years. This can only happen via better understanding and earlier recognition of underlying mechanisms for developing SDB and an intensive collaboration between different medical specialities.

Acknowledgments

We thank the voluntary children and their parents who participated in the present study. We are also most indebted to the PANIC Study researchers for their skillful contribution in performing the study. This work has been financially supported by grants from the Ministry of Social Affairs and Health of Finland, the Ministry of Education and Culture of Finland the Finnish Innovation Fund Sitra, the Social Insurance Institution of Finland, the Finnish Cultural Foundation, the Juho Vainio Foundation, the Foundation for Paediatric Research, the Paavo Nurmi Foundation and the Kuopio University Hospital (EVO-funding number 5031343).

Conflict of interest

The authors declare that there is no conflict of interests.

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Tiina Ikävalko
    • 1
    • 2
  • Henri Tuomilehto
    • 3
  • Riitta Pahkala
    • 1
    • 2
  • Tuomo Tompuri
    • 4
    • 5
  • Tomi Laitinen
    • 5
  • Riitta Myllykangas
    • 1
  • Anu Vierola
    • 4
  • Virpi Lindi
    • 4
  • Matti Närhi
    • 2
    • 4
  • Timo A. Lakka
    • 4
    • 6
  1. 1.Oral and Maxillofacial DepartmentKuopio University HospitalKuopioFinland
  2. 2.Institute of DentistryUniversity of Eastern FinlandKuopioFinland
  3. 3.Department of OtorhinolaryngologyKuopio University HospitalKuopioFinland
  4. 4.Department of Physiology, Institute of BiomedicineUniversity of Eastern FinlandKuopioFinland
  5. 5.Department of Clinical Physiology and Nuclear MedicineKuopio University Hospital and University of Eastern FinlandKuopioFinland
  6. 6.Kuopio Research Institute of Exercise MedicineKuopioFinland

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