Pulmonary function and sleep-related breathing disorders in severely obese children

doi:10.1016/j.clnu.2005.12.001

Clinical Nutrition

Volume 25, Issue 5, October 2006, Pages 803-809

https://doi.org/10.1016/j.clnu.2005.12.001 Get rights and content

Summary

Background & aims

To evaluate the frequency of pulmonary function and sleep-breathing disorders in severely obese children and to search for their association with obesity phenotypes.

Methods

Sleep studies and spirometry were performed for 54 severely obese children.

Results

Upper airway resistances (RAWs) were increased with RAW>200% and forced 25 s expiratory volume<80% in 83% and 60% of individuals, respectively. A decrease in functional residual capacity (FRC)<80% was found in 43%. Fifty-two percent of the children had a desaturation index>10 during sleep, and 41% of children presented at least one of three severity criteria (snoring index>300 per hour, respiratory events index (REI)>10 and arousal index>10). Univariate analyses showed a positive correlation between snoring index and BMI Z-score and neck/height ratio ( $P = 0.01$ and $0.04$ , respectively) as between REI and the same parameters ( $P = 0.01$ and $0.03$ , respectively). In a multivariate model with BMI Z-score, NHR still correlated with the snoring index ( $P = 0.02$ ) and REI ( $P = 0.01$ ).

Conclusions

In our cohort, obese children showed frequent pulmonary function and sleep-breathing disorders. The later were associated with impaired upper airway respiratory conductance.

Introduction

The prevalence of childhood obesity is increasing at an alarming rate in western countries resulting from an interaction between environmental factors and genes.1, 2 Childhood obesity is associated with morbidity and significant risk for the development of cardiovascular and related diseases in later life,3, 4 justifying the necessity to detect such complications as early as possible.

In obese adults, both pulmonary function and sleep-breathing disorders are well known and are related to the severity of obesity.⁵ The most frequently reported abnormalities in pulmonary function are reductions in lung volumes and expiratory flow rates, mainly caused by the mass of visceral fat, which show positive results following weight loss.⁶ Sleeping disorders such as obstructive sleep apnoea (OSA) in obese adults are also a major problem because of increased cardiovascular and cerebrovascular morbidity.⁷ Development of OSA is multifactorial, including body fat distribution, sex, and structural differences in upper airway dimensions.8, 9 There is also a link between OSA and insulin resistance,¹⁰ and hyperleptinaemia is associated with OSA in obese adult patients independently of body mass index (BMI) suggesting a role of leptin resistance in obesity-related breathing disorders.¹¹

For children, the few studies that have evaluated the effect of obesity on pulmonary function have showed conflicting results. Reductions in functional residual capacity (FRC) and impaired diffusion have been described as the commonest abnormalities in obese children, with a correlation between the reduction in static lung volume and the degree of obesity.¹² However, others found that obstructive abnormalities were the main problem, while some studies did not detect significant pulmonary disorders.13, 14 These conflicting results justify the necessity to explore pulmonary function in obese children to clarify the frequency and nature of such disorders.

OSA episodes are prevalent in obese children, but they are less severe than in adults.13, 15, 16, 17, 18, 19 As in adults, the risk of developing OSA increases with the severity of obesity and is related to complications such as behavioural problems, learning difficulties, inhibition in normal growth patterns, cardiovascular abnormalities (elevated diastolic blood pressure)²⁰ and even insulin resistance.¹⁷ However, in the absence of specific symptoms related to OSA except for snoring, such disorders could be underestimated in obese children with potential long-term consequences during later life, especially in the absence of specific therapeutic measures such as adenotonsillectomy or continuous positive airway pressure (CPAP).²¹ In addition, the mechanisms inducing OSA in obese children are unknown except for the severity of obesity, as in adults, justifying the necessity to evaluate such disorders in obese children. Furthermore, only two studies have evaluated both pulmonary and nocturnal functions in the same group of such children.13, 16

The aim of our study was to evaluate the frequency of pulmonary function and sleep-breathing disorders in a cohort of severely obese children and to evaluate their association with clinical symptoms related to OSA, to the severity of obesity, to fat-mass repartition, and to metabolic complications.

Section snippets

Study population

Fifty-four children with severe obesity were recruited consecutively and prospectively at our Outpatient Department of Paediatric Nutrition from 2002 to 2004 (Table 1). Severe obesity was defined as a BMI Z-score>3 SD over mean age- and sex-specific BMI values determined in French children by Rolland-Cachera.²² Patients with syndromic obesity such as Prader–Willi or Laurence–Moon–Biedl syndromes, were excluded. All included patients were recruited for severe obesity with or without nocturnal

Patient characteristics

Results of anthropometry, body composition and laboratory tests are shown in Table 1. Thirty-six patients were Caucasians (67%) and 18 Blacks (33%). Thirteen patients were prepubertal (26%) and 37 pubertal (74%). Concerning clinical symptoms, 23% of the patients had morning headaches, 33% reported diurnal somnolence, 53% had nocturnal agitation with nocturnal perspiration in 42% of cases, 77% had a history of snoring, and 19% had a previous history of asthma.

Pulmonary studies

Pulmonary studies were performed for

Discussion

We evaluated the frequency of pulmonary function and sleep-breathing disorders in this cohort of severely obese children and searched for their association with specific phenotypes related to obesity. We found that both were already frequent in severely obese children, and that impaired respiratory conductance in upper airways was the main factor related to OSA in severely obese children.

In this study, we showed that OSA was a major concern in these obese children. We used an REI threshold>10

Acknowledgements

We thank Yves Lebouc and his staff (Endocrinology Laboratory, Armand-Trousseau Hospital) for performing the plasma glucose, insulin, and leptin measurements.

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This result could be due to the small effect in each group. Reduction in plethysmographic functional residual capacity (FRC) is the most consistently reported effect of obesity on lung function, particularly in morbidly obese children [4,23]. Correlations between BMI z-score and reduction of FRC are not unanimously consistent in the literature.
To assess the respiratory function and sleep characteristics of obese adults and children.
All patients with non-syndromic, severe obesity (BMI ≥ 3 z-scores for children and ≥ 40.00 kg/m² for adults), referred for pulmonary function tests at Lille University Hospital, were retrospectively included.
A total of 69 children (mean ± SD BMI 36.8 ± 6.7 and mean BMI z-score 4.7 ± 1.0) and 70 adults were included (mean BMI 45.7 ± 6.2). Metabolic syndrome was diagnosed in 13 children (26%) and 40 adults (80%). Reduced lung volumes were observed in 34 children (50.0%) and 16 adults (24.0%) and both the mean functional residual capacity (FRC) and the mean residual volume (RV) were lower in children than in adults (FRC: −1.7 ± 2.1 z-score in children vs. −1.0 ± 1.1 in adults, P = 0.026; and RV: −0.8 ± 1.2 z-score in children vs. −0.1 ± 1.1 in adults, P = 0.002). The prevalence of severe obstructive sleep apnea syndrome was greater in adults (40.7% vs. 18.8%, P = 0.007). Children had a higher average oxygen saturation (median of 96.0% [91.0–98.0] vs. 93.0% [76.0–97.0] in adults, P < 0.0001).
Obesity has consequences for lung volumes in children; however, a longitudinal study is needed to determine the impact on pulmonary expansion and growth.
Inhaled albuterol increases estimated ventilatory capacity in nonasthmatic children without and with obesity
2021, Respiratory Physiology and Neurobiology
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It is also unknown if an increase in FEF25−75 with a bronchodilator could have an important impact on estimated ventilatory capacity between 25 and 75 % of vital capacity (V̇Ecap25−75), especially in children with obesity, whose breathing mechanics may be altered at rest and during exercise. In children with obesity, extra weight on the chest wall reduces functional residual capacity (FRC) at rest and end-expiratory lung volume (EELV) during exercise to a point that is closer to residual volume (RV) where maximal expiratory flow is lowest (Dubern et al., 2006; Mendelson et al., 2012; Davidson et al., 2014) and expiratory flow limitation (EFL, an indicator of ventilatory limitation) is more likely to occur (Gibson et al., 2014; Mendelson et al., 2012). For example, FRC was reduced by 30 % (p < 0.05) in a group of adolescent children with obesity, when compared with their normal weight counterparts (Mendelson et al., 2012).
Forced mid-expiratory flow (i.e., isoFEF₂₅₋₇₅) may increase with a short-acting β₂-agonist in nonasthmatic children without bronchodilator responsiveness. This could also increase estimated ventilatory capacity along mid-expiration (V̇Ecap₂₅₋₇₅), especially in vulnerable children with obesity who exhibit altered breathing mechanics. We estimated V̇Ecap₂₅₋₇₅ pre- and post-albuterol treatment in 8−12yo children without (n = 28) and with (n = 46) obesity. A two-way ANOVA was performed to determine effects of an inhaled bronchodilator (pre-post) and obesity (group) on isoFEF₂₅₋₇₅ and V̇Ecap₂₅₋₇₅. There was no group by bronchodilator interaction or main group effect on outcome variables. However, a significant main effect of the bronchodilator was detected in spirometry parameters, including a substantial increase in isoFEF₂₅₋₇₅ (17.1 ± 18.0 %) and only a slight (non-clinical) but significant increase in FEV₁ (2.4 ± 4.3 %). V̇Ecap₂₅₋₇₅ significantly increased with albuterol (+11.7 ± 10.6 L/min; +15.8 ± 13.9 %). These findings imply potentially important increases in ventilatory reserve with a bronchodilator in nonasthmatic children without and with obesity, which could potentially influence respiratory function at rest and during exercise.
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La surcharge pondérale chez l’enfant et l’adolescent se définit par un indice de masse corporelle (IMC) supérieur au 97^e percentile pour l’âge et le sexe selon des courbes établies par l’International Obesity Task Force (IOTF). On estime qu’en France, elle toucherait 25 % des moins de 18 ans. Elle est d’origine multifactorielle, avec une influence importante de facteurs génétiques, modulée par des déterminants précoces pré et post-nataux (tabagisme maternel, etc.), sociétaux et psychologiques. L’impact fonctionnel respiratoire de l’obésité chez l’enfant se traduit essentiellement par une diminution du rapport VEMS/CVF. Plusieurs études ont par ailleurs montré une association entre asthme et surpoids/obésité, avec un impact péjoratif de l’IMC sur le contrôle de l’asthme. Cependant, l’asthme est encore mal caractérisé dans cette population et les déterminants de l’obstruction bronchique semblent être différents de ceux des enfants non obèses, avec notamment peu d’inflammation éosinophile. Le syndrome d’apnées obstructives du sommeil (SAOS) est une complication fréquente du surpoids et toucherait jusqu’à 80 % des enfants et adolescents obèses. Il a une définition polysomnographique spécifique chez l’enfant. La symptomatologie est globalement la même que chez l’adulte, avec cependant des altérations cognitives et/ou neurocomportementales souvent plus marquées chez l’adolescent. Le traitement repose sur la chirurgie ORL lorsqu’elle est indiquée (avec réalisation d’une polysomnographie postopératoire), puis sur la ventilation par pression positive continue (PPC). Le syndrome d’obésité-hypoventilation (SOH), enfin, a la même définition chez l’enfant que chez l’adulte et toucherait environ 20 % des patients. Son traitement repose sur la ventilation nocturne à deux niveaux de pression. Dans certains cas extrêmes chez l’adolescent, la chirurgie bariatrique peut être proposée. L’indication devra être posée dans un centre spécialisé à compétence pédiatrique.
In childhood and adolescence overweight is defined as a body mass index (BMI) above the 97th percentile for age and sex, according to the curves established by the International Obesity Task Force (IOTF). In France, it is estimated that 25 % of children under 18 years old are overweight. Overweight and obesity in this population are multifactorial, with an important influence of genetic factors, modulated by pre and post-natal (maternal smoking), societal and psychological determinants. The impact of obesity on respiratory function in children is mostly characterized by a decreased FEV1/FCV. Moreover, several studies have shown an association between asthma and overweight/obesity, with a pejorative impact of BMI on asthma control. However, asthma is still poorly characterized in this population, and the determinants of bronchial obstruction seem to differ from non-obese children, with less eosinophilic inflammation. Obstructive sleep apnea syndrome (OSAS) is a frequent complication of obesity, affecting up to 80% of obese children and adolescents. It has a specific polysomnographic definition in children. Symptoms are similar to adult OSAS, but with cognitive and neurobehavioral alterations often more important in adolescents. The treatment consists in ENT surgery when indicated (with systematic post-operative polysomnography), and nocturnal continuous positive airway pressure (CPAP). The obesity-hypoventilation syndrome (OHS) has the same definition in children as in adults and affects up to 20% of obese patients. Treatment consists in nocturnal ventilation using bilevel positive airway pressure (BiPAP). Finally, in some extreme cases, bariatric surgery can be performed. The indication should be discussed in a specialised paediatric reference centre.
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Research in the last few decades has shown that obesity and its metabolic complications have important effects on the respiratory system. There is ample and growing evidence that obesity affects lung function in otherwise healthy adults and children. Obesity exerts an additional load upon the respiratory system, changing the balance of pressures between the inward recoil of the lung and the outward pressure of the chest. This has major consequences on lung volumes, airway mechanics, airway closure, expiratory flow limitation, ventilation distribution, airway hyperresponsiveness, and exhaled nitric oxide levels. Many of the changes in lung function due to obesity are likely to contribute to respiratory symptoms; however, there are important differences in the effect of obesity on lung function between children, adolescents, and adults. Therefore understanding the effects of obesity on lung function throughout the lifespan is imperative to understanding present and future effects of obesity on respiratory health.
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To assess the effects of obesity on lung volume and capacity in children and adolescents.
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Of the 1,030 articles, only four were included in the review. The studies amounted to 548 participants, predominantly males, with sample size ranging from 45 to 327 individuals. 100% of the studies evaluated nutritional status through BMI (z‐score) and 50.0% reported the data on abdominal circumference. All demonstrated that obesity causes negative effects on lung volume and capacity, causing a reduction mainly in functional residual capacity in 75.0% of the studies; in the expiratory reserve volume in 50.0% and in the residual volume in 25.0%. The methodological quality ranged from moderate to high, with 75.0% of the studies classified as having high methodological quality.
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ORIGINAL ARTICLEPulmonary function and sleep-related breathing disorders in severely obese children

Summary

Background & aims

Methods

Results

Conclusions

Introduction

Section snippets

Study population

Patient characteristics

Pulmonary studies

Discussion

Acknowledgements

J Pediatr

Lancet

Am J Med Sci

Chest

Chest

J Pediatr

J Pediatr

Respir Physiol

Chest

Lancet

J Pediatr

Genetics of body-weight regulation

Nature

Risks and consequences of childhood and adolescent obesity

Int J Obes Relat Metab Disorders

Cardiovascular risk factors in patients with obstructive sleep apnoea syndrome

Eur Respir J

Neck and total body fat deposition in nonobese and obese patients with sleep apnea compared with that in control subjects

Am J Respir Crit Care Med

Obstructive sleep apnoea is independently associated with insulin resistance

Am J Respir Crit Care Med

Plasma leptin levels and cardiac sympathetic function in patients with obstructive sleep apnoea–hypopnoea syndrome

Thorax

ORIGINAL ARTICLE
Pulmonary function and sleep-related breathing disorders in severely obese children