DOI 10.1378/chest.09-1529 2010;137;1085-1090; Prepublished online February 5, 2010;Chest
and Lucio ArmenioColella, Maurizio Delvecchio, Vito Paolo Logrillo, Ruggiero Francavilla Luigia Brunetti, Riccardina Tesse, Vito Leonardo Miniello, Isabella Children : The Southern Italy ExperienceSleep-Disordered Breathing in Obese
written permission of the copyright holder.this article or PDF may be reproduced or distributed without the priorDundee Road, Northbrook, IL 60062. All rights reserved. No part of Copyright2010by the American College of Chest Physicians, 3300Physicians. It has been published monthly since 1935.
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The interplay between obesity and respiratory function has implications for sleep-disordered
breathing (SDB) in childhood. Horner et al 1 have documented in adults that fatty infi ltration of upper airway structures causes upper airway narrowing,
whereas subcutaneous fat deposits in the anterior neck region and other cervical structures exert collapsing forces that promote increased pharyngeal collapsibility. Although a similar assessment of the airway structures and dynamics in obese children remains to be done, there is strong evidence to suggest that structural differences in upper airway dimension in combination with large tonsils and adenoids can make airway obstruction a signifi cant concern in obese children. Moreover, obesity can affect ventilation
Background: The association of obesity with sleep-associated respiratory disturbances, which has traditionally been described as a problem in adults, actually originates in childhood. We sought an association between sleep-disordered breathing (SDB) and overweight and/or obesity in a large cohort of school- and preschool-aged children in Southern Italy. Methods: One thousand two hundred seven children (612 girls and 595 boys ; mean age 7.3 years) were screened by self-administered questionnaires. According to answers, subjects were divided into three groups: nonsnorers (NS), occasional snorers (OS), and habitual snorers (HS). All HS, who also failed an oximetry study at home, underwent polysomnographic monitoring for the defi -nition of SDB. BMI was calculated according to Italian growth charts. Results: A total of 809 subjects (67.0%) were eligible for the study. Of them, 44 subjects (5.4%) were classifi ed as HS, 138 (17.0%) as OS, and 627 (77.5%) as NS. Fourteen subjects (1.7%) were given a diagnosis of obstructive sleep apnea syndrome (OSAS). Sixty-four subjects (7.9%) were defi ned as obese, 121 (14.9%) as overweight, and 624 (77.2%) as normal weight. The frequency of HS was signifi cantly higher in obese subjects than in overweight and normal-weight subjects (12.5% vs 5.8% vs 4.6%, respectively ; P 5 .02), whereas the frequency of OSAS was 1.6% in normal-weight, 1.6% in overweight, and 3.1% in obese subjects ( P 5 not signifi cant). Conclusions: Our fi ndings in a large sample of Italian children suggest that obesity is associated with snoring. CHEST 2010; 137(5):1085–1090
Manuscript received June 29, 2009; revision accepted January 12, 2010. Affi liations: From the Department of Biomedicine of the Develop-mental Age, Pediatric Unit “S. Maggiore” (Drs Brunetti, Tesse, Miniello, Colella, Logrillo, and Armenio), University of Bari, Bari; Pediatric Unit-IRCCS “Casa Sollievo della Sofferenza” (Dr Delvecchio), San Giovanni Rotondo, Foggia; and the Department of Biomedi-cine of the Developmental Age, Pediatric Unit “B. Trambusti” (Dr Francavilla), University of Bari, Bari, Italy. Correspondence to: Luigia Brunetti, MD, Clinica Pediatrica “S. Maggiore,” Policlinico, University of Bari, Piazza Giulio Cesare, 11-70124 Bari, Italy; e-mail: [email protected]
distinct phases: a screening phase, which aimed to select children with a history suggestive of sleep breathing anomalies, and a sec-ond investigative phase. In light of the latest epidemic data on obesity, which have prompted remarkable changes in the propor-tion of obese children who are referred for SDB, the present study investigated patients’ auxologic characteristics within cate-gories of snorers.
All procedures used were in accordance with the guidelines of the Helsinki Declaration on Human Experimentation. The study was carried out in accordance with the Provincial Education Offi ce of Bari and the local school Ethics Committee. Informed consent at enrollment was obtained from all parents.
Screening Phase
A 41-item multiple-choice questionnaire was distributed to children at school. It was formulated according to Brouillette’s guidelines revised by Carroll. 6,7,29 The questionnaire inquired about family history for atopy, child medical history, snoring and/or apneas (frequency and duration), presence of symptoms that could be related to breathing disorders (troubled sleep, enuresis, thirst, sweating, oral breathing, need of afternoon rest, daily sleepiness, poor school achievement), and smoking habits in the family and during pregnancy ( . 20 cigarettes/d). In the sleep sec-tion, questions were structured to score the severity of sleep-related symptoms according to a four-point scale, as described previously. 14 In the following statistical evaluation, scores of 3 (always) were defi ned as habitual snorers (HS), scores of 2 (some-times) as occasional snorers (OS), and scores of 1 (seldom) or 0 (never) as nonsnorers (NS). Families that did not return the ques-tionnaires were contacted by phone on two separate occasions (15 days apart) before being classifi ed as nonresponders.
Second Phase
Only HS entered the second phase of the study. Subjects were offered an instrumental defi nition of the disorder for the diagno-sis of either OSAS or primary snoring. Instrumental tests were undertaken while the children had no upper-airway infections. A device (Vitalog HMS 5000, Pocket Polygraph; Markos srl; Monza; Italy) was used for a nighttime home evaluation. In accor-dance with the American Sleep Disorders Association’s screen-ing methodologies, 30 the following parameters were monitored: (1) transcutaneous saturation of oxygen, (2) heart rate (through ECG), (3) snoring, and (4) body position. For the evaluation of snoring, a microphone was positioned over the larynx.
Following the Italian guidelines for the diagnosis of childhood OSAS, recordings with an oxygen desaturation index (ODI) (ODI 5 the number of signifi cant desaturations [ � . 4%] per hours of sleep) . 2 were regarded as suggestive of OSAS, and subjects were then considered eligible for nocturnal polygraphic monitoring (NPM). 31,32 The NPM was recorded in the sleep labo-ratory of our unit. Our clinic is the tertiary referral center for the diagnosis and follow-up of SDB in Southern Italy, covering an estimated population of 1.4 million children, with . 700 children followed up in our sleep clinic.
Polysomnography was performed overnight. The device used for NPM was the Vitalog HMS 5000. The conditions of measure-ments and the parameters monitored are described elsewhere. 14 Obstructive apnea was defi ned as absent airfl ow in the presence of respiratory effort for at least two respiratory cycle times, accom-panied by at least a 4% decrease in arterial oxygen saturation. Obstructive hypopnea was defi ned as a decrease of at least 50% in the amplitude of the oronasal thermistor signal, with maintained respiratory effort for at least two respiratory cycle times, accompa-nied by a � 4% decrease in arterial oxygen saturation. 31 The apnea/hypopnea index (AHI) was calculated as (No. of obstructive apnea
through mass loading of the respiratory system. 2,3 Increased adipose tissue in the abdominal wall and cavity, as well as that surrounding the thorax, reduces intrathoracic volume and diaphragm excursion, par-ticularly in the supine position, and increases the work of breathing during sleep. 4,5
SDB exists in a continuous spectrum from snoring to severe obstructive sleep apnea syndrome (OSAS) and, because nearly all children affected by OSAS snore, it is necessary to distinguish between the two conditions. Primary snoring, a common fi nding in childhood, is not associated with the typical features of OSAS, such as apnea, oxygen desaturation, or hyperventilation, but it may precede complex SBD by many years. 6,7 Epidemiologic data of SDB, and particularly OSAS, in childhood are limited 8-13 ; we have recently reported the prevalence of this condi-tion in a large cohort of Italian children. 14
On the other hand, the prevalence of childhood obesity has risen worldwide over the last quarter cen-tury, especially in the United States, 15 and, although not well studied, it can be assumed that the increased prevalence of obesity has also been accompanied by a rise in the incidence of SDB. The excess body fat in children is also associated with the earlier emergence of metabolic conditions, such as insulin resistance and type 2 diabetes mellitus, systemic hypertension, and dyslipidemia, 16-20 and some authors have suggested the presence of a subclinical infl am-mation in overweight children with OSAS and have speculated that OSAS exacerbates the chronic infl ammatory state that characterizes obese adipose tissue. 21-24
How childhood obesity is associated with SDB and what contribution the breathing disorder might play in maintaining obesity and increasing the risk of comorbidities are still debated among researchers worldwide. 25-28 The available data on children do not support straightforward conclusions, mainly because of methodologic differences among studies con-ducted in different countries. In this cross-sectional study, we sought a relationship between overweight or obesity and sleep breathing disturbances in a large sample of children, using Italian thresholds for the identifi cation of childhood SDB.
Materials and Methods
This study is a further analysis of a previous larger epidemio-logic survey about sleep-related disorders in childhood in South-ern Italy. 14 We enrolled 1,207 children, and we stratifi ed them by school attended and by year of course. In each stratum, classes were randomly selected, and students in each class were enrolled. Six hundred twelve subjects (51%) were female, and 595 (49%) were male (mean age, 7.3 years; range, 3-11 years); 379 subjects (31%) were in nursery schools and 828 (69%) were in primary schools. This cross-sectional prevalence study was designed in two
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121 subjects (14.9%), and in the range of obesity in 64 subjects (7.9%). There was no difference in BMI between male and female subjects.
Sleep Disorders and Body Weight
The frequency of snorers according to body weight, as reported in Table 2 , showed no signifi cant differ-ence. However, when we considered NS and OS in the same subgroup, the frequency of HS was signifi -cantly higher in obese subjects than in subjects who were overweight and of normal weight (12.5% vs 5.8% vs 4.6%, respectively; P 5 .02, Table 3 ). The fre-quency of OSAS was 1.6% in normal-weight, 1.6% in overweight, and 3.1% in obese subjects ( P 5 not signifi cant). The regression analysis showed that BMI may explain the presence of snoring with an odds ratio of 2.81 (95% CI, 1.15-6.36; P , .01).
Discussion
There is compelling evidence from the literature that obese children and adolescents are prone to develop SDB. 35-42 There is a wide difference in the prevalence of these disorders among the various stud-ies, likely related to a number of factors, such as ethnicity and different diagnostic criteria for OSAS and obesity. Our cross-sectional study represents a large-scale assessment of the association between obesity and SDB in Italian children. In HS, we found a signifi cantly higher percentage of obese (12.5%) than overweight (5.8%) and normal-weight subjects (4.6%). We observed a prevalence of obesity of 3.1% among patients affected by OSAS.
Most studies performed so far in a smaller sample size showed a higher prevalence of OSAS in obese children. Guilleminault et al 36 reported that 10% of 50 children with a diagnosis of OSAS were obese. Marcus et al 37 and Mallory et al 38 showed polysomno-graphic abnormalities in 24% of 41 and in 46% of 22 obese young subjects, respectively . Similarly, Silvestri et al 39 documented evidence of partial airway obstruction in 66% and complete airway obstruction in 59% of 32 obese children. In addition, Redline et al 35 observed that for every increment in BMI by
events 1 No. of obstructive hypopnea events) per hour of sleep time. Subjects with an AHI . 3 received a diagnosis of mild-to-severe OSAS. 14 The nadir of oxygen and the percentage of total sleep time with arterial oxygen saturation , 90% were also calculated.
All subjects were weighed and measured by specifi cally trained personnel. Standing height was evaluated with a wall-mounted Harpenden Stadiometer (Holtain Ltd; Dyfed, Wales). With patients in underwear, weight was measured with an electronic scale with digital readings accurate to 0.1 kg. BMI was calculated by dividing weight in kilograms by the square of height in meters. Height and weight were expressed in SD scores according to the Italian growth charts. 33 Overweight and obesity were defi ned by the methods sug-gested by Cole, 34 according to the cutoff values calculated for the Italian population. 33
Statistical Analysis
Statistical analysis was performed with SPSS software, release 15.0 for Windows (SPSS Inc., Chicago, IL). Data were expressed as mean 6 SD. Analysis of variance and the x 2 test were used to compare mean values and frequencies among groups. For 2 3 2 tables, Fisher exact test was computed when a frequency was expected to be , 5. The role of obesity as a prognostic factor for SDB was analyzed by logistic regression. P , .05 was considered statistically signifi cant.
Results
Questionnaire and NPM Results
From the previously published cohort, 809 subjects attending nursery and primary school were eligible for this study. Four hundred two subjects (49.7%) were male and 407 (50.3%) were female (chronologic age, 7.7 6 2.2 years; range, 3.1-11.3 years).
After evaluation of the questionnaires, 44 subjects (5.4%) were classifi ed as HS, 138 (17.1%) as OS, and 627 (77.5%) as NS. The percentage of HS, OS, and NS was not different on the basis of gender ( Table 1 ).
Of the 44 HS subjects who underwent home instrumental evaluation, 24 (54.5%) with an ODI . 2 were considered for NPM. Fourteen patients (10 boys and four girls) received a diagnosis of OSAS, and the prevalence of this disorder in the studied cohort was 1.7%.
Body Weight Evaluation
BMI was within the normal limits for age and sex in 624 subjects (77.2%), in the range of overweight in
Table 1— Distribution of the Study Population in Habitual Snorers, Occasional Snorers, and
Nonsnorers by Gender
Gender
Snorers
NS OS HS
Boys 302 72 28Girls 325 66 16
P value 5 not signifi cant. HS 5 habitual snorers; NS 5 nonsnorers; OS 5 occasional snorers.
Table 2— Distribution of the Study Population in Habitual Snorers, Occasional Snorers, and
sented a very small proportion of the total number of respiratory events, and thus we do not think their presence altered our conclusions. Fourth, scoring of SDB events in this study was performed using data from thermistors, although their use it is not recom-mended as the primary fl ow monitor in children. 48
Despite the aforementioned limitations, this study gives additional data about the relationship between overweight or obesity and sleep-breathing distur-bances in children, using Italian thresholds for the identifi cation of childhood SDB. Additional strengths are the large size of the cohort, the use of a commu-nity sample in lieu of a clinic-derived cohort, and the use of home NPM instead of the parent report only.
Adenotonsillar hyperplasia/hypertrophy is not always the main contributing factor to the development of SDB in obese children. 49 Upper airway narrowing may also result from fatty infi ltration of upper airway structures. 1 Moreover, obesity has several effects on the respiratory system; in particular, it leads to a decline in the expiratory reserve volume and an increase in the FEV 1 /FVC ratio. 50 Increased adipose tissue in the abdominal wall and cavity and surround-ing the thorax increases the global respiratory load. 2-4
In the context of obesity contributions to the emer-gence of SDB in children, the role played by adipok-ines, in particular leptin, in the pathophysiology of upper airway resistance and altered ventilatory responses has been investigated recently. Obesity is associated with peripheral and central leptin resis-tance, which, in turn, leads to a relatively ineffective elevation of circulating leptin levels. 51 The reduced bioavailability of leptin has been implicated in dimin-ished hypercapnic responses and in mechanisms underlying alveolar hypoventilation in obesity. 52
Conclusions
In conclusion, obese subjects are up to six times more likely than lean subjects to be snorers and to have other symptoms of sleep-related obstructed breathing, 53 which are independently related to the development of hypertension, cardiovascular dis-eases, behavioral disorders, poor school performance in children, daytime sleepiness, and poor quality of life in adults. 54 On the other hand, it is acknowledged that obese children and adolescents are prone to become obese adults, and that the risk of developing metabolic disorders depends strictly on weight during childhood. It suggests that an obese HS in childhood might have a greater risk of becoming an obese adult with sleep disorders, further increasing the risk of comorbidities. Thus, we think that sleep disorders should be taken into serious consideration by pedia-tricians to prevent comorbidities in adulthood.
1 kg/m 2 beyond mean BMI for age and gender, the risk of OSAS increased by 12%. Wing et al 40 reported that 33% of obese children had OSAS. Verhulst et al 27 estimated a prevalence of 19% OSAS among obese children and of 41% in overweight children. In a study from Singapore, Chay et al 41 reported that 21% of 86 obese children had an AHI of more than fi ve episodes per hour.
Several caveats should be considered in the inter-pretation of our study. First, although we propose an AHI cutoff point . 3 for the patient’s diagnostic defi -nition of OSAS, it is likely that we have underesti-mated the degree of SDB in this population. The lack of an accepted standard for AHI to indicate the severity of SDB in children has important implica-tions and it makes diffi cult the comparison of research studies using different defi nitions. A number of AHI thresholds have been used, ranging from 1 to 10, with varying requirements for associated oxygen desaturation. 32,42,43 From a clinical perspective, it becomes a factor hindering identifi cation of SDB in children. In the aforementioned fi rst such study in children, Marcus et al 32 found apneic events to be rare and suggested that an apnea index � 1 was abnormal. However, hypopneas were not scored. Subsequently, several studies reported that apneas and hypopneas were uncommon in younger children, but event defi nitions were not always comparable among all studies. 43-47 Mallory 38 and Chay 41 set a high AHI, . 5, to defi ne OSAS pediatric patients in their studies. 27 It remains unclear whether any of these AHI thresholds is superior to others. This continues to be an area that requires additional investigation.
Second, because not all HS, and no OS or NS sub-jects, were studied by NPM, a considerable number of OSAS patients may have been missed. In fact, by selecting HS subjects to undergo NPM according to a strict ODI value, we have presumably considered patients with more severe forms of OSAS. Moreover, while fi lling out the questionnaire, not all parents knew that their children snored, even if they were trained by clinicians to recognize symptoms suggestive for snoring and OSAS. Third, although central apneas were not included in our defi nition of AHI, they repre-
Table 3— Distribution of the Study Population in Habitual Snorers and Occasional Snorers Plus
Nonsnorers by BMI
BMI
Snorers
OS and NS HS
Normal weight 595 29Overweight 114 7Obese 56 8
P value obese vs overweight vs normal weight 5 .02. See Table 1 for expansion of abbreviations.
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Acknowledgments Author contributions: Dr Brunetti: contributed to study design and interpretation of results. Dr Tesse: contributed to the preparation of the manuscript and to data analysis. Dr Miniello: contributed to the interpretation of the results of the study. Dr Colella: contributed to data collection and the preparation of the manuscript. Dr Delvecchio: contributed to statistical data analysis. Dr Logrillo: contributed to data collection and instrumental mon-itoring technical assistance. Dr Francavilla: contributed to interpretation of the results of the study and to data analysis. Dr Armenio: contributed to study design, supervision of the work, and manuscript preparation. Financial/nonfi nancial disclosures: The authors have reported to CHEST that no potential confl icts of interest exist with any companies/organizations whose products or services may be discussed in this article .
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