- Email: [email protected]
Longitudinal Impact of Resolution of Snoring in Young Children on Psychosocial Functioning
Longitudinal Impact of Resolution of Snoring in Young Children on Psychosocial Functioning Sarah N. Biggs, PhD1,2, Lisa M. Walter, PhD1,2, Angela R. Jackman, PhD3, Lauren C. Nisbet, MBBS, PhD1, Aidan J. Weichard, BSc (Hons)1, Samantha L. Hollis, BA (Hons)1, Margot J. Davey, MBBS1,2,4, Vicki Anderson, PhD5, Gillian M. Nixon, MD1,2,4, and Rosemary S. C. Horne, PhD1,2 Objective To determine whether sustained resolution of sleep disordered breathing (SDB) in young children, either because of treatment or spontaneous recovery, predicted long-term improvements in quality of life, family functioning, and parental stress. Study design Children diagnosed with primary snoring (n = 16), mild obstructive sleep apnea (OSA, n = 11), moderate-severe (MS) OSA (n = 8), and healthy nonsnoring controls (n = 25) at ages 3-5 years underwent repeat polysomnography at 6-8 years. Parents completed quality of life and parental stress questionnaires at both time points. Resolution of SDB was determined as obstructive apnea hypopnea index (OAHI) #1 event/hour, or absence of snoring during polysomnography or on parent report. Linear mixed-model analyses determined the effects of resolution on psychosocial morbidity. OAHI was used to determine the predictive value of changes in SDB severity on psychosocial outcomes. Results Fifty percent of primary snoring, 45% mild OSA, and 63% MS OSA resolved, of which 67% received treatment. Children originally diagnosed with SDB continued to show significant psychosocial impairments compared with nonsnoring controls, irrespective of resolution. A reduction in OAHI predicted improvements in physical symptoms, school functioning, family worry and family relationships, and stress related to a difficult child. Conclusions Treatment was more likely to result in resolution of SDB if original symptoms were MS. Children originally diagnosed with SDB, irrespective of resolution, continued to experience psychosocial dysfunction suggesting additional interventions are required. (J Pediatr 2015;167:1272-79).
S
leep disordered breathing (SDB) is common in children and ranges in severity from primary snoring, characterized by habitual snoring with no gas exchange abnormalities or sleep fragmentation, to severe obstructive sleep apnea (OSA), characterized by hypoxemia, hypercapnia, and frequent arousals from sleep.1,2 SDB in children is predominantly caused by enlarged tonsils and adenoids with prevalence peaking during the preschool years when the size of pharynx is at its smallest compared with the lymphoid tissue.2,3 A second peak during adolescence has been observed more recently, which has been attributed to the increasing prevalence of childhood obesity.4 Research has shown that SDB in children, irrespective of severity, carries a high psychosocial morbidity including increased behavioral problems,5-7 reduced quality of life (QOL),8-11 poorer family relationships,9,10 and increased parental stress.10 Treatment efficacy studies have shown a marked improvement in QOL for children,12-18 however, these studies have predominantly had short-term follow-up periods,13,15,16,18 have not objectively assessed SDB or examined effects of severity of disease,18 or have not compared the results with children with SDB who did not receive treatment.17 The most common treatment for OSA in children is removal of the tonsils and/or adenoids19 but surgical, and to some extent, medical treatment is not common in children with primary snoring, despite demonstrated morbidity. In addition, treatment efficacy studies are confounded as surgery does not always resolve sleep and breathing problems, and a proportion of children who are not treated will spontaneously resolve.20-22 This study aimed to determine whether sustained resolution of SDB, either because of treatment or spontaneous, that was originally diagnosed during the
Child PedsQL Family PedsQL HRQOL MS NREM OAHI OSA
PedsQL 4.0 Generic Core Scales Parent-Report 36-item PedsQL Family Impact Module Health-related QOL Moderate-severe Non-REM Obstructive apnea hypopnea index Obstructive sleep apnea
PedsQL PSG PSI QOL REM SDB SRI TST
Pediatric Quality of Life Inventory Polysomnography Parenting stress index Quality of life Rapid eye movement Sleep disordered breathing Social risk index Total sleep time
From the 1The Ritchie Center, Hudson Institute of Medical Research; 2Department of Pediatrics, Monash University; 3Melbourne School of Psychological Sciences, University of Melbourne; 4Melbourne Children’s Sleep Center, Monash Children’s Hospital, Monash Medical Center; and 5Clinical Sciences Research, Murdoch Children’s Research Institute, Melbourne, Australia Funded by the National Health and Medical Research Council of Australia (APP491001 and APP1008919) and the Victorian Government’s Operational Infrastructure Support Program. The authors declare no conflicts of interest. 0022-3476/$ - see front matter. Copyright ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jpeds.2015.09.016
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Methods The Monash Health and Monash University Human Research Ethics Committees granted ethical approval. Written informed consent and verbal assent was obtained from parents and children, respectively. Children (n = 160, 3-5 years of age) without comorbid conditions, clinically referred to the Melbourne Children’s Sleep Center for assessment of SDB, and age-matched, nonsnoring controls (n = 42), recruited through community advertisements, underwent overnight polysomnography (PSG) and psychometric testing between 2008 and 2011.6,10,23-25 A total of 115 children with SDB and 38 nonsnoring controls had complete PSG and psychosocial data at baseline and were eligible to participate in the current study.10 Parents were informed of the longitudinal nature of the study at baseline, and annual newsletters were sent as a reminder of their intent to return. Three years following the baseline study, families were invited to return for follow-up. A proportion of children with SDB received treatment following the initial baseline study. The decision to treat was made by parents in consultation with their treating physician and was independent of this study. Parents who declined to return were asked the reasons for refusal, what treatment, if any, their child received following the baseline study, and the child’s current snoring status. Protocol The protocols for the baseline and follow-up studies were identical. Children underwent 1 overnight PSG. Height and weight were measured and converted to a body mass index z-score to adjust for sex and age.26 Questionnaires relating to demographics, general health, and behavior were completed by parents on the night of the PSG. Questionnaires pertaining to QOL, family functioning, and parental stress were completed during the psychometric testing, which was conducted in the home approximately 3 weeks (mean SD = 19 11 days) following the PSG. Both parents and the researcher were blinded to the results of the followup PSG at the time the questionnaires and psychometric testing were completed. PSG Electrophysiological signals were recorded using a commercially available PSG system (E-Series; Compumedics, Melbourne, Australia) using standard pediatric recording techniques as previously described.6,10 Studies were manually sleep-staged into 30-second epochs, and respiratory events scored by experienced pediatric sleep technologists using standard clinical protocols.27,28 Sleep variables included sleep onset latency (time from lights out to first epoch of sleep), wake after sleep onset (percentage of time awake from first epoch of sleep to end of study), total
sleep time (TST, time asleep from first epoch of sleep to end of study), sleep efficiency (wake after sleep onset/TST expressed as a percentage) and percentage of TST spent in nonrapid eye movement (REM) (NREM) sleep, consisting of 3 stages of increasing sleep depth (N1, N2, N3), and REM sleep. Severity of SDB was determined using the obstructive apnea hypopnea index (OAHI). The OAHI was defined as the total number of obstructive apneas (full obstruction), mixed apneas (both central and obstructive), obstructive hypopneas, and respiratory events related arousal or desaturation (partial obstruction) per hour of TST. Criteria for the categorization of SDB severity were primary snoring-OAHI #1 event/hour with a clinical history of snoring; mild OSA-OAHI >1-5 events/hour; or moderate-severe (MS) OSA-OAHI >5 events/hour. At follow-up, all children originally diagnosed with SDB, regardless of severity, were combined and divided into 2 groups according to whether their SDB had resolved (resolved, unresolved). SDB was considered resolved if OAHI #1, there was no snoring reported during the PSG, and no snoring was reported on the OSA-18 questionnaire. Any child with an OAHI >1 event/hour or any child with primary snoring with an OAHI #1 event/hour but who continued to snore were categorized as unresolved. Demographic Information Family structure, parental level of education, parental occupation, maternal age at child’s birth, and English language exposure were recorded. Socioeconomic status was determined using the social risk index (SRI),29 as described previously.6 The SRI provides an indication of social and economic status (range 0-12, with 0 indicating highest status) based on 6 key aspects: family structure, highest education completed by primary caregiver, employment status of primary income earner, occupation of primary income earner, language spoken in the home, and maternal age at the birth of the child. Maternal occupation was converted to an occupational status score developed from the Census of 2006.30 This score ranges from 0-100 with a higher score indicative of higher occupational prestige. QOL Assessment The OSA-18, specifically designed to assess QOL associated with SDB, determined health-related QOL (HRQOL).31 The items are scored on a 7-point Likert scale anchored by 1 = none of the time; and 7 = all of the time and grouped into 5 domains: sleep disturbance, physical symptoms, emotional symptoms, daytime functioning, and caregiver concerns. A total score less than 60 suggests the child’s SDB has a small impact on HRQOL, between 60 and 80 indicates a moderate impact, and greater than 80 indicates a large impact. The scores from the individual domains and total score at follow-up were subtracted from the scores at baseline to determine the change score. A negative change score indicates a deterioration of HRQOL, whereas a positive change score indicates an improvement. 1273
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Change scores of <0.5 indicates no change, 0.5-0.9 a small change, 1.0-1.4 a moderate change, and >1.4 a large change.32 General QOL was assessed with the Pediatric Quality of Life Inventory (PedsQL) 4.0 Generic Core Scales ParentReport (henceforth called “child PedsQL”).33 The child PedsQL is a 21-item (aged 2-4 years) or 23-item (aged 512 years) questionnaire that provides 4 functional domains (physical, emotional, social, and school) and 2 summary scales (psychosocial health and total score). Item scores were linearly transformed to a scale of 0-100, with higher scores representing better QOL. Age standardized z-scores were calculated using published normative data.34 Parent HRQOL and family functioning were assessed using the 36-item PedsQL Family Impact Module (henceforth called “family PedsQL”).35 This questionnaire contains 8 subscales (physical, emotional, social and cognitive functioning, communication, worry, daily activities, and family relationships), which are summed to provide a summary score for parent HRQOL, family functioning, and total score. Item scores were transformed as detailed above. Normative data is not available for this module. All questionnaires have been shown to be sensitive to detecting changes following adenotonsillectomy in children with SDB.8,18 Parental Stress Assessment The level of parental stress was assessed using the parenting stress index (PSI), third edition, short form.36 This 36-item self-report questionnaire provides 3 subscales (parental distress, parent-child dysfunction, and difficult child) and a total stress score. An indication of the level of defensive responding is also provided to account for reporter bias. Raw scores were converted to centiles for analysis. Statistical Analyses Statistical analyses were performed using SPSS (IBM Statistics v 20; SPSS Inc, Chicago, Illinois). Data were tested for normality and equal variance. All respiratory variables showed a positive skew and were analyzed using nonparametric analyses. Continuous demographic data were analyzed using repeated measures ANOVA. Categorical data were assessed using c2 analysis. Group differences in PSG recorded sleep variables over time were analyzed with repeated measures ANOVA with Bonferroni post-hoc testing where ANOVA was significant (P < .05). Differences in respiratory variables were assessed using Kruskal-Wallis ANOVA on ranks, with Mann-Whitney U post-hoc testing where appropriate (P < .05). Linear mixed-model analyses were used to determine the fixed effects of time and resolution of SDB on QOL and parental stress outcomes. OAHI was entered as a covariate to determine the predictive value of changes in SDB severity on changes in psychosocial outcomes. Subject was used as the random effect, accounting for interindividual differences. Group differences in the change in scores in the OSA-18 and child PedsQL were analyzed using a 1-way ANOVA. 1274
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Results At follow-up, 19% of the original cohort could not be contacted, 41% declined further participation, and 2 controls were ineligible as they were diagnosed with a behavioral disorder following the baseline study. Reasons for refusal included the original referral issue had resolved and their child did not need a repeat sleep study (49%); the child refused to participate (18%); parent was too busy (12%); parental illness or accident (7%); parent was unhappy with the clinical process at baseline (7%); or the family had moved outside the metropolitan area (7%). Seven percent did not provide a reason for refusal. Final response rate was 30% for the children originally diagnosed with SDB and 68% for the control group. Two control children were subsequently excluded from analysis because of developing SDB. The proportion of children who were treated was not significantly different between the children who returned and those who did not (P = .15). There were no differences in age, sex, body mass index z-score, maternal occupation, or maternal education between those that refused and those that returned. The SRI was higher in those who did not return (mean SD = 1.4 1.7) compared with those who did return (mean SD = 0.8 1.1, P = .016), indicating that those who refused were from a slightly lower socioeconomic background. There were no differences in any of the psychosocial domains at baseline between participating and nonparticipating children with SDB at follow-up. The families of nonsnoring control children scored higher on the domain of cognitive functioning (indicating better functioning) on the family PedsQL questionnaire (t [17.3] = 2.2, P = .037) and scored lower on parental distress (indicated less distress) (t [36] = 2.0, P = .049) at baseline than the nonsnoring controls that did not return. Demographics As can be seen in Figure 1 (available at www.jpeds.com), 29% of children originally diagnosed with primary snoring, 31% with mild OSA, and 33% with MS OSA returned. Of these, 38% of children with primary snoring, 55% with mild OSA and 100% with MS OSA were treated. Of those that were treated, 33% of children with primary snoring, 50% with mild OSA, and 63% with MS OSA resolved. Spontaneous resolution also occurred in 60% of children with primary snoring and 40% with mild OSA. In total, 51% (18/35) of children originally diagnosed with SDB had resolved and 49% (17/35) had ongoing SDB. Furthermore, 90% (18/20) of the treated children underwent surgery for removal of tonsils and/or adenoids, and 10% (2/20, both mild OSA) received medical treatment in the form of nasal steroids (Table I). Sleep and Respiratory Variables All children slept more than 5 hours during the PSG on both the baseline (mean SD = 443 37 minutes) and follow-up (mean SD = 429 47 minutes) studies. Changes in sleep Biggs et al
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Table I. Cohort demographics Control (N = 25) Age (y: mean SD) BMI z-score (mean SD) Sex (N, % male) Maternal education (N, % tertiary educated) Maternal occupation (mean SD, range 0-100) English language exposure (N, % English only) SRI (mean SD)
Resolved (N = 18)
Unresolved (N = 17)
Baseline
Follow-up
Baseline
Follow-up
Baseline
Follow-up
P
4.2 (1.1) 0.5 (1.2)
7.5 (1.1) 0.4 (0.9) 11 (44) 18 (72) 74 (19) 23 (92) 0.4 (0.9)
4.6 (0.8) 0.7 (1.2)
7.8 (0.9) 0.7 (0.8) 15 (83) 7 (39) 58 (17) 11 (61) 1.2 (1.5)
4.2 (0.8) 0.6 (1.0)
7.3 (0.9) 0.3 (1.0) 8 (47) 12 (75) 67 (19) 11 (65) 0.9 (1.1)
NS* NS* .02† .03† .02z NS† .02x
BMI, body mass index; NS, nonsignificant. *Repeated measures ANOVA: significance value of group main effect reported. †c2 analysis. zOne-way ANOVA. xKruskal-Wallis ANOVA on ranks.
variables over time were as expected with increasing age. Overall %N1 (F [1,56] = 10.1, P = .002), % total REM (F [1,56] = 4.9, P = .03), and sleep efficiency (F [1,56] = 6.4, P = .02) decreased over time. Overall %N2 (F [1,56] = 37.1, P < .001), % total NREM (F [1,56] = 5.6, P = .02), and % wake after sleep onset (F [1,56] = 9.4, P = .003) increased over time. At both baseline and follow-up, children in the control group obtained more NREM (F [1,56] = 5.3, P = .008) and less REM (F [1,56] = 5.0, P = .01) than the children in the resolved group. There were no differences in sleep variables between the control and unresolved groups. There were no significant interactions between group and time indicating that there was no effect of resolution of SDB on the change in sleep variables over time. By design, significant differences in OAHI between the control and resolved groups at baseline were no longer evident at follow-up. OAHI remained significantly higher in the unresolved group compared with the control group (Mann-Whitney U = 49.5, P < .001) and became significantly higher than the resolved group (Mann-Whitney U = 44.0, P < .001) at follow-up. This pattern was also observed in the arousal index. Oxygen saturation improved for all groups over time. Psychosocial Outcomes Table II shows the means and 95% CIs for all psychosocial outcome measures. A higher score on both the OSA-18 and PSI indicate poorer psychosocial functioning. Conversely, higher scores on the child and family PedsQL indicate better QOL. OSA-18 The mixed-model analysis revealed a significant effect of group for all HRQOL measures (Table II). Mean scores were significantly higher, indicating poorer HRQOL, in both the resolved and unresolved groups than control for the domains of sleep disturbance, physical symptoms, emotional symptoms, daytime functioning, and caregiver concern. There were no differences between the resolved and unresolved groups. There was a significant improvement of HRQOL sleep disturbance at follow-up
compared with baseline. Post-hoc analysis revealed that the resolved group had significantly greater improvement in sleep disturbance, daytime functioning and caregiver concern than the unresolved group. Analysis of the change scores shows a large change in sleep disturbance, a moderate change in physical symptoms and caregiver concern, and a small, nonsignificant, change in emotional symptoms and daytime functioning in the resolved group compared with the unresolved and control groups (Figure 2, A). A reduction in OAHI significantly predicted an improvement in physical symptoms (b = 0.2, P = .001), but not on any other subscale. PedsQL Overall, scores on the child and family PedsQL remained unchanged between baseline and follow-up (Table II). Post-hoc analyses revealed that for all domains, except family social functioning, there were no differences between the resolved and unresolved groups, however, both groups scored significantly lower (ie, worse general QOL) than the control group. For family social functioning, scores were not different between the control and unresolved groups, with both groups scoring significantly higher (ie, better general QOL) than the resolved group. Figure 2, B shows the change in z-score from baseline to follow-up in the child PedsQL. A change in OAHI was significantly, negatively related to school functioning on the child PedsQL questionnaire, with a decrease in OAHI predicting an increase in school functioning (b = 2.4, P = .026). A change in OAHI was also significantly negatively related to worry and family relationships on the family PedsQL questionnaire, with a decrease in OAHI predicting an improvement in QOL related to family worry (ie, less worry: b = 2.5, P = .043) and family relationships (ie, improved relationships: b = 3.7, P < .01). Parental Stress Mixed model results for the PSI are shown in Table II. Overall levels of parental stress did not change between baseline and follow-up, irrespective of whether SDB had
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Table II. Results of mixed model analysis for OSA-18, PedsQL, and parental stress index Results of mixed model fixed effects Control
OSA-18 Sleep disturbance Physical symptoms Emotional symptoms Daytime functioning Caregiver concern Total score Child PedsQL Physical Emotional Social School Psychosocial health Total Family PedsQL Physical Emotional Social Cognition Communication Worry Daily activities Family relationships Parent health Family summary Total PSI Parental distress Parent-child dysfunction Difficult child Total stress
Resolved
Unresolved
Time
Group
Time group
Baseline
Follow-up
Baseline
Follow-up
Baseline
Follow-up
F
F
F
1.3 (1.2-1.5) 1.6 (1.4-1.8) 2.3 (1.9-2.6) 1.5 (1.3-1.7) 1.2 (1.1-1.3) 27 (25-29)
1.2 (1.0-1.3) 1.3 (1.1-1.4) 1.8 (1.4-2.2) 1.3 (1.1-1.4) 1.2 (1.0-1.5) 24 (21-26)
4.0 (3.4-4.6) 3.5 (2.6-4.3) 3.8 (3.1-4.4) 3.2 (2.7-3.6) 3.6 (2.7-4.5) 66 (56-76)
2.0 (1.4-2.5) 2.3 (1.7-2.8) 3.0 (2.3-3.7) 2.3 (1.6-3.0) 2.3 (1.5-3.1) 41 (32-50)
3.5 (2.9-4.1) 2.8 (2.2-3.3) 3.4 (2.8-4.1) 2.8 (2.2-3.3) 2.8 (2.3-3.4) 54 (47-62)
2.8 (2.3-3.3) 2.8 (2.2-3.4) 3.2 (2.2-4.1) 2.7 (2.3-3.2) 2.7 (2.0-3.3) 50 (42-59)
5.6* 2.1 0.2 2.0 1.1 1.8
45.8†,z 14.1†,z 9.7†,z 30.4†,z 27.1†,z 37.0†,z
10.8† 2.6 1.3 3.4* 4.2* 7.9x
93 (90-96) 87 (83-92) 92 (86-98) 94 (89-98) 91 (87-95) 91 (88-95)
95 (92-98) 83 (76-89) 93 (88-98) 92 (88-95) 89 (85-93) 91 (88-95)
82 (74-91) 66 (58-73) 82 (72-91) 82 (73-91) 75 (69-82) 78 (72-85)
78 (67-89) 67 (55-78) 82 (72-91) 74 (62-85) 74 (65-83) 75 (66-85)
82 (75-89) 64 (54-74) 83 (75-91) 86 (78-94) 77 (70-83) 78 (72-85)
84 (78-89) 65 (53-76) 80 (74-87) 73 (65-80) 72 (66-79) 77 (71-82)
0.2 0.1 2.8 0.7 0.8 0.4
10.4†,{ 12.3†,{ 5.7x,{ 8.3x,{ 13.1†,{ 14.0†,{
0.9 0.7 0.0 0.5 0.1 0.2
93 (90-96) 93 (89-98) 95 (90-99) 96 (93-99) 97 (95-100) 98 (96-99) 92 (85-99) 94 (90-98) 95 (91-97) 95 (92-97) 95 (92-97)
94 (89-98) 93 (88-98) 98 (96-100) 94 (90-98) 99 (97-100) 96 (93-100) 93 (88-99) 95 (90-99) 95 (91-98) 94 (90-99) 95 (92-98)
69 (61-77) 76 (66-85) 78 (70-88) 76 (65-87) 82 (73-91) 70 (57-83) 67 (56-78) 74 (64-85) 74 (66-82) 72 (62-81) 74 (66-81)
75 (64-86) 75 (64-86) 83 (70-96) 78 (65-92) 82 (96-94) 78 (68-88) 69 (55-84) 76 (63-89) 78 (67-88) 74 (61-86) 77 (67-87)
76 (69-84) 79 (71-87) 88 (82-94) 80 (72-89) 84 (76-91) 81 (73-89) 67 (54-81) 75 (63-87) 80 (74-86) 71 (62-85) 78 (72-85)
79 (70-88) 77 (67-87) 86 (74-98) 82 (69-95) 82 (72-92) 82 (73-91) 74 (61-88) 73 (61-86) 81 (71-90) 74 (62-86) 79 (71-88)
2.0 0.4 0.7 0.1 0.1 1.0 0.1 0.2 0.2 0.1 0.1
21.4†,{ 9.4†,{ 8.5x,** 8.0x,{ 10.8†,{ 12.6†,{ 9.0†,{ 7.3x,{ 16.0†,{ 10.0†,{ 18.3†,{
1.4 0.2 0.4 0.7 0.1 0.9 0.9 1.1 0.8 0.9 1.2
42 (28-57) 42 (27-56) 46 (30-61) 40 (37)
19 (9-29) 26 (16-36) 26 (15-38) 19 (26)
43 (27-59) 44 (28-59) 62 (48-77) 57 (33)
35 (19-51) 45 (27-64) 55 (36-75) 48 (36)
42 (25-59) 49 (34-64) 59 (43-75) 49 (35)
48 (33-63) 54 (36-72) 63 (46-80) 62 (31)
1.1 0.0 0.1 0.9
1.3 2.8 7.5†,z 6.0x,††
0.4 0.1 0.2 0.2
F, ratio of between group variance to within group variance. Data for the OSA-18 are presented as raw scores. The linearly transformed score of 0-100 is presented for PedsQL, and centiles are presented for PSI. All data are presented as mean (95% CI). *P < .05. †P < .001. zControl < resolved = unresolved. xP < .01. {Control > resolved = unresolved. **Control > resolved. ††Control < unresolved.
resolved. Post-hoc analyses of group differences showed parents indicated more stress relating to a difficult child in both the resolved and unresolved groups compared with the control group. Parents of children with unresolved SDB reported significantly more total stress than parents of control children. A change in OAHI was significantly, negatively associated with a change in scores for stress related to a difficult child (b = 1.9, P = .048), indicating that an improvement in OAHI was predictive of decreased scores on the difficult child scale (ie, less difficult).
Discussion This study revealed that a reduction in respiratory obstruction, as measured by the OAHI, was associated with an improvement in some aspects of QOL, family functioning, and parental stress, yet complete resolution of SDB did not 1276
normalize these outcomes. With little exception, psychosocial functioning remained poorer in children originally diagnosed with SDB than nonsnoring controls, irrespective of resolution. The OSA-18 showed an improvement in domains specifically relating to SDB severity in children whose SDB had resolved compared with the unresolved group, however, impairments in domains of general functioning such as emotional symptoms and daytime functioning remained. This was also reflected in the PedsQL and parental stress measures, with resolution having no impact on any change in scores from baseline to follow-up on the PedsQL or PSI. The continued psychosocial impairment in children originally diagnosed with SDB in the current study is consistent with behavioral data reported in our previous study of school-aged children.20 This could imply that any insult during early development because of SDB is irreversible. Alternatively, these results support the referral bias theory that states parents of children with mild forms of SDB seek medical investigation because of concomitant behavioral issues rather Biggs et al
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Figure 2. Group differences in A, change in domain scores of the OSA-18 and B, child PedsQL. A positive score indicates an improvement from baseline to follow-up. A negative score indicates poorer functioning. Data are mean and SEs. *P < .05. † P < .01. zP < .001.
than concerns about sleep per se. If behavioral difficulties were the mediator of psychosocial outcomes, resolution of the respiratory symptoms may not result in long-term improvements. Current clinical treatment decisions are based on a number of factors including clinical history, physical examination including the size of the lymphoid tissue, and when available, the metrics assessed by PSG.2 Clinical evidence supports surgical intervention for MS OSA, but if PSG metrics, such as OAHI, sleep fragmentation, and oxygen desaturation, do not show significant OSA, surgical treatment is not usually prescribed, primarily because of the risks involved with the procedure.37 This study supports previous research that has consistently shown these metrics to be poor predictors of behavioral,5,6,38 cognitive,7,39 and psychosocial
dysfunction.10,15 Most recently, the Childhood Adenotonsillectomy Trial showed that although children with OSA (mean Obstructive Respiratory Disturbance Index <8 events/hour) randomized into the early tonsillectomy group, showed improved QOL 7 months after surgery compared with those in the watchful waiting group, these improvements were only minimally explained by changes in PSG variables.15 Combined, these and the current results add to the mounting evidence that alternate assessment variables are needed for children with milder forms of SDB. Despite no difference in psychosocial impairment between the children who resolved and those that did not at followup, this study does show a significant relationship between a reduction in OAHI and outcomes relating to family
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functioning and parental stress. It was recently shown that school-aged children with MS OSA had greater improvement in OSA-18 sleep disturbance, caregiver concern, and total score than those with mild OSA or primary snoring.17 Although that study did not include a posttreatment PSG, rendering it impossible to determine if any of the treated children had residual disease, it does suggest that improvement in psychosocial outcomes are dependent on disease severity. In contrast, the Tucson Children’s Assessment of Sleep Apnea study showed that having persistent SDB from childhood to early adolescence significantly increased the odds of behavioral and adaptive dysfunction.40 In the current study, the greatest reduction in OAHI was observed in children originally diagnosed with MS OSA, irrespective of whether they met our definition for resolution. Treatment, surgical or otherwise, is not routinely recommended for children with primary snoring and is only occasionally recommended for children with mild OSA, unless significant adenotonsillar hypertrophy is present.2 Our data support these current treatment practices, however, as children with milder SDB appear less likely to resolve with treatment, and as those with unresolved SDB continue to experience poor psychosocial outcomes, alternate or additional treatment or interventions for children with mild forms of SDB are required. The primary limitation of this study was the low response rate, with those refusing participation outnumbering those who agreed. Although nonresponders had similar demographic backgrounds, treatment history, and psychosocial outcomes at baseline to responders, selection bias is a possibility. The low response also resulted in the study being underpowered to effectively examine changes in psychosocial functioning by severity and resolution. Finally, we were unable to determine the impact of untreated MS OSA on outcomes as all participants originally diagnosed with MS OSA were treated. Nonetheless, the examination of psychosocial outcomes following complete resolution of SDB rather than simply by treatment is a strength of this study. It is now understood that treatment, surgical or otherwise, does not always result in resolution of SDB both in the short22 and long term.20,21 Although preliminary, by eliminating the confounder of residual disease on long-term outcomes in the analysis, this study provides a greater understanding of the efficacy of treatment and ongoing psychosocial dysfunction in children with SDB. This study shows that children with SDB, irrespective of resolution, continue to experience psychosocial dysfunction over the long term. Future research examining alternate or additional interventions to improve psychosocial outcomes in children with SDB, is an essential next step in this field. n We thank Mark Tacey for his statistical advice. Submitted for publication Apr 29, 2015; last revision received Jul 14, 2015; accepted Sep 3, 2015.
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Vol. 167, No. 6 Reprint requests: Sarah N. Biggs, PhD, The Ritchie Center, Level 5 Monash Medical Center, Level 5, 246 Clayton Rd, Clayton, Victoria 3168, Australia. E-mail: [email protected]
References 1. Katz ES, D’Ambrosio CM. Pathophysiology of pediatric obstructive sleep apnea. Proc Am Thorac Soc 2008;5:253-62. 2. Marcus CL, Brooks LJ, Draper KA, Gozal D, Halbower AC, Jones J, et al. Diagnosis and management of childhood obstructive sleep apnea syndrome. Pediatrics 2012;130:576-84. 3. Jeans WD, Fernando DC, Maw AR, Leighton BC. A longitudinal study of the growth of the nasopharynx and its contents in normal children. Br J Radiol 1981;54:117-21. 4. Spilsbury JC, Storfer-Isser A, Rosen CL, Redline S. Remission and incidence of obstructive sleep apnea from middle childhood to late adolescence. Sleep 2015;38:23-9. 5. Bourke RS, Anderson V, Yang JS, Jackman AR, Killedar A, Nixon GM, et al. Neurobehavioral function is impaired in children with all severities of sleep disordered breathing. Sleep Med 2011;12:222-9. 6. Jackman AR, Biggs SN, Walter LM, Embuldeniya US, Davey MJ, Nixon GM, et al. Sleep-disordered breathing in preschool children is associated with behavioral, but not cognitive, impairments. Sleep Med 2012;13:621-31. 7. Miano S, Paolino MC, Urbano A, Parisi P, Massolo AC, Castaldo R, et al. Neurocognitive assessment and sleep analysis in children with sleepdisordered breathing. Clin Neurophysiol 2011;122:311-9. 8. Baldassari CM, Mitchell RB, Schubert C, Rudnick EF. Pediatric obstructive sleep apnea and quality of life: a meta-analysis. Otolaryngol Head Neck Surg 2008;138:265-73. 9. Crabtree VM, Varni JW, Gozal D. Health-related quality of life and depressive symptoms in children with suspected sleep-disordered breathing. Sleep 2004;27:1131-8. 10. Jackman AR, Biggs SN, Walter LM, Embuldeniya US, Davey MJ, Nixon GM, et al. Sleep disordered breathing in early childhood: quality of life for children and families. Sleep 2013;36:1639-46. 11. Rosen CL, Palermo TM, Larkin EK, Redline S. Health-related quality of life and sleep-disordered breathing in children. Sleep 2002;25:657-66. 12. Constantin E, Kermack A, Nixon GM, Tidmarsh L, Ducharme FM, Brouillette RT. Adenotonsillectomy improves sleep, breathing, and quality of life but not behavior. J Pediatr 2007;150:540-6. 6.e1. 13. Ericsson E, Lundeborg I, Hultcrantz E. Child behavior and quality of life before and after tonsillectomy versus tonsillectomy. Int J Pediatr Otorhinolaryngol 2009;73:1254-62. 14. Flanary VA. Long-term effect of adenotonsillectomy on quality of life in pediatric patients. Laryngoscope 2003;113:1639-44. 15. Garetz SL, Mitchell RB, Parker PD, Moore RH, Rosen CL, Giordani B, et al. Quality of life and obstructive sleep apnea symptoms after pediatric adenotonsillectomy. Pediatrics 2015;135:e477-86. 16. Goldstein NA, Fatima M, Campbell TF, Rosenfeld RM. Child behavior and quality of life before and after tonsillectomy and adenoidectomy. Arch Otolaryngol Head Neck Surg 2002;128:770-5. 17. Lee CH, Kang KT, Weng WC, Lee PL, Hsu WC. Quality of life after adenotonsillectomy for children with sleep-disordered breathing: a linear mixed model analysis. Int J Pediatr Otorhinolaryngol 2014;78:1374-80. 18. Mohsen N, Susan A, Shahin B, Soheila D. Sleep related quality of life before and after adenotonsillar surgery in pediatric population. Int J Pediatr Otorhinolaryngol 2014;78:330-3. 19. Marcus CL, Brooks LJ, Draper KA, Gozal D, Halbower AC, Jones J, et al. Diagnosis and management of childhood obstructive sleep apnea syndrome. Pediatrics 2012;130:e714-55. 20. Biggs SN, Vlahandonis A, Anderson V, Bourke R, Nixon GM, Davey MJ, et al. Long-term changes in neurocognition and behavior following treatment of sleep disordered breathing in school-aged children. Sleep 2014;37:77-84.
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December 2015 21. Huang YS, Guilleminault C, Lee LA, Lin CH, Hwang FM. Treatment outcomes of adenotonsillectomy for children with obstructive sleep apnea: a prospective longitudinal study. Sleep 2014;37:71-6. 22. Marcus CL, Moore RH, Rosen CL, Giordani B, Garetz SL, Taylor HG, et al. A randomized trial of adenotonsillectomy for childhood sleep apnea. N Engl J Med 2013;368:2366-76. 23. Nisbet LC, Yiallourou SR, Biggs SN, Nixon GM, Davey MJ, Trinder JA, et al. Preschool children with obstructive sleep apnea: the beginnings of elevated blood pressure? Sleep 2013;36:1219-26. 24. Nisbet LC, Yiallourou SR, Nixon GM, Biggs SN, Davey MJ, Trinder J, et al. Characterization of the acute pulse transit time response to obstructive apneas and hypopneas in preschool children with sleep-disordered breathing. Sleep Med 2013;14:1123-31. 25. Nisbet LC, Yiallourou SR, Nixon GM, Biggs SN, Davey MJ, Trinder J, et al. Nocturnal autonomic function in preschool children with sleepdisordered breathing. Sleep Med 2013;14:1310-6. 26. Ogden C, Kuczmarski R, Flegal K, Mei Z, Guo S, Wei R, et al. Centers for disease control and prevention 2000 growth charts for the United States: improvements to the 1977 national center for health statistics version. Pediatrics 2002;109:45-60. 27. Iber C, Ancoli-Israel S, Chesson A Jr, Quan SF. The AASM manual for the scoring of sleep and associated events: Rules, terminology and technical specifications. Manchester, IL: American Academy of Sleep Medicine; 2007. 28. Nixon GM, Hyde M, Biggs SN, Walter LM, Horne RS, Davey MJ. The impact of recent changes to the respiratory scoring rules in pediatrics. J Clin Sleep Med 2014;10:1217-21. 29. Roberts G, Howard K, Spittle AJ, Brown NC, Anderson PJ, Doyle LW. Rates of early intervention services in very preterm children with developmental disabilities at age 2 years. J Paediatr Child Health 2008; 44:276-80. 30. McMillan J, Beavis A, Jones F. The AUSEI06: a new socioeconomic index for Australia. J Sociol 2009;45:123-49.
31. Franco RA Jr, Rosenfeld RM, Rao M. First place—resident clinical science award 1999. Quality of life for children with obstructive sleep apnea. Otolaryngol Head Neck Surg 2000;123:9-16. 32. Sohm H, Rosenfeld RM. Evaluation of sleep-disordered breathing in children. Annual Meeting of the American Academy of Otolaryngology-Head and Neck Surgery; Sept 9-12, 2001. Denver, CO: American Academy of Otolaryngology; 2003. 33. Varni JW, Burwinkle TM, Seid M, Skarr D. The PedsQL 4.0 as a pediatric population health measure: feasibility, reliability, and validity. Ambul Pediatr 2003;3:329-41. 34. Varni JW, Limbers CA, Burwinkle TM. Parent proxy-report of their children’s health-related quality of life: an analysis of 13 878 parents’ reliability and validity across age subgroups using the PedsQL 4.0 Generic Core Scales. Health Qual Life Outcomes 2007;5:2. 35. Varni JW, Sherman SA, Burwinkle TM, Dickinson PE, Dixon P. The PedsQL Family Impact Module: preliminary reliability and validity. Health Qual Life Outcomes 2004;2:55. 36. Abidin R. The parenting stress index. Professional manual. 3rd ed. Lutz, FL: Psychological Assessment Resources; 1995. 37. Konstantinopoulou S, Gallagher P, Elden L, Garetz SL, Mitchell RB, Redline S, et al. Complications of adenotonsillectomy for obstructive sleep apnea in school-aged children. Int J Pediatr Otorhinolaryngol 2015;79:240-5. 38. Beebe DW, Wells CT, Jeffries J, Chini B, Kalra M, Amin R. Neuropsychological effects of pediatric obstructive sleep apnea. J Int Neuropsychol Soc 2004;10:962-75. 39. Bourke R, Anderson V, Yang JS, Jackman AR, Killedar A, Nixon GM, et al. Cognitive and academic functions are impaired in children with all severities of sleep-disordered breathing. Sleep Med 2011;12:489-96. 40. Perfect MM, Archbold K, Goodwin JL, Levine-Donnerstein D, Quan SF. Risk of behavioral and adaptive functioning difficulties in youth with previous and current sleep disordered breathing. Sleep 2013;36: 517-525B.
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Figure 1. Flow chart depicting response rate from baseline to follow-up, the proportion of children in each sleep disorder breathing group that were treated, and the proportion of those who were treated that were resolved at follow-up.
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S
leep disordered breathing (SDB) is common in children and ranges in severity from primary snoring, characterized by habitual snoring with no gas exchange abnormalities or sleep fragmentation, to severe obstructive sleep apnea (OSA), characterized by hypoxemia, hypercapnia, and frequent arousals from sleep.1,2 SDB in children is predominantly caused by enlarged tonsils and adenoids with prevalence peaking during the preschool years when the size of pharynx is at its smallest compared with the lymphoid tissue.2,3 A second peak during adolescence has been observed more recently, which has been attributed to the increasing prevalence of childhood obesity.4 Research has shown that SDB in children, irrespective of severity, carries a high psychosocial morbidity including increased behavioral problems,5-7 reduced quality of life (QOL),8-11 poorer family relationships,9,10 and increased parental stress.10 Treatment efficacy studies have shown a marked improvement in QOL for children,12-18 however, these studies have predominantly had short-term follow-up periods,13,15,16,18 have not objectively assessed SDB or examined effects of severity of disease,18 or have not compared the results with children with SDB who did not receive treatment.17 The most common treatment for OSA in children is removal of the tonsils and/or adenoids19 but surgical, and to some extent, medical treatment is not common in children with primary snoring, despite demonstrated morbidity. In addition, treatment efficacy studies are confounded as surgery does not always resolve sleep and breathing problems, and a proportion of children who are not treated will spontaneously resolve.20-22 This study aimed to determine whether sustained resolution of SDB, either because of treatment or spontaneous, that was originally diagnosed during the
Child PedsQL Family PedsQL HRQOL MS NREM OAHI OSA
PedsQL 4.0 Generic Core Scales Parent-Report 36-item PedsQL Family Impact Module Health-related QOL Moderate-severe Non-REM Obstructive apnea hypopnea index Obstructive sleep apnea
PedsQL PSG PSI QOL REM SDB SRI TST
Pediatric Quality of Life Inventory Polysomnography Parenting stress index Quality of life Rapid eye movement Sleep disordered breathing Social risk index Total sleep time
From the 1The Ritchie Center, Hudson Institute of Medical Research; 2Department of Pediatrics, Monash University; 3Melbourne School of Psychological Sciences, University of Melbourne; 4Melbourne Children’s Sleep Center, Monash Children’s Hospital, Monash Medical Center; and 5Clinical Sciences Research, Murdoch Children’s Research Institute, Melbourne, Australia Funded by the National Health and Medical Research Council of Australia (APP491001 and APP1008919) and the Victorian Government’s Operational Infrastructure Support Program. The authors declare no conflicts of interest. 0022-3476/$ - see front matter. Copyright ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jpeds.2015.09.016
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Methods The Monash Health and Monash University Human Research Ethics Committees granted ethical approval. Written informed consent and verbal assent was obtained from parents and children, respectively. Children (n = 160, 3-5 years of age) without comorbid conditions, clinically referred to the Melbourne Children’s Sleep Center for assessment of SDB, and age-matched, nonsnoring controls (n = 42), recruited through community advertisements, underwent overnight polysomnography (PSG) and psychometric testing between 2008 and 2011.6,10,23-25 A total of 115 children with SDB and 38 nonsnoring controls had complete PSG and psychosocial data at baseline and were eligible to participate in the current study.10 Parents were informed of the longitudinal nature of the study at baseline, and annual newsletters were sent as a reminder of their intent to return. Three years following the baseline study, families were invited to return for follow-up. A proportion of children with SDB received treatment following the initial baseline study. The decision to treat was made by parents in consultation with their treating physician and was independent of this study. Parents who declined to return were asked the reasons for refusal, what treatment, if any, their child received following the baseline study, and the child’s current snoring status. Protocol The protocols for the baseline and follow-up studies were identical. Children underwent 1 overnight PSG. Height and weight were measured and converted to a body mass index z-score to adjust for sex and age.26 Questionnaires relating to demographics, general health, and behavior were completed by parents on the night of the PSG. Questionnaires pertaining to QOL, family functioning, and parental stress were completed during the psychometric testing, which was conducted in the home approximately 3 weeks (mean SD = 19 11 days) following the PSG. Both parents and the researcher were blinded to the results of the followup PSG at the time the questionnaires and psychometric testing were completed. PSG Electrophysiological signals were recorded using a commercially available PSG system (E-Series; Compumedics, Melbourne, Australia) using standard pediatric recording techniques as previously described.6,10 Studies were manually sleep-staged into 30-second epochs, and respiratory events scored by experienced pediatric sleep technologists using standard clinical protocols.27,28 Sleep variables included sleep onset latency (time from lights out to first epoch of sleep), wake after sleep onset (percentage of time awake from first epoch of sleep to end of study), total
sleep time (TST, time asleep from first epoch of sleep to end of study), sleep efficiency (wake after sleep onset/TST expressed as a percentage) and percentage of TST spent in nonrapid eye movement (REM) (NREM) sleep, consisting of 3 stages of increasing sleep depth (N1, N2, N3), and REM sleep. Severity of SDB was determined using the obstructive apnea hypopnea index (OAHI). The OAHI was defined as the total number of obstructive apneas (full obstruction), mixed apneas (both central and obstructive), obstructive hypopneas, and respiratory events related arousal or desaturation (partial obstruction) per hour of TST. Criteria for the categorization of SDB severity were primary snoring-OAHI #1 event/hour with a clinical history of snoring; mild OSA-OAHI >1-5 events/hour; or moderate-severe (MS) OSA-OAHI >5 events/hour. At follow-up, all children originally diagnosed with SDB, regardless of severity, were combined and divided into 2 groups according to whether their SDB had resolved (resolved, unresolved). SDB was considered resolved if OAHI #1, there was no snoring reported during the PSG, and no snoring was reported on the OSA-18 questionnaire. Any child with an OAHI >1 event/hour or any child with primary snoring with an OAHI #1 event/hour but who continued to snore were categorized as unresolved. Demographic Information Family structure, parental level of education, parental occupation, maternal age at child’s birth, and English language exposure were recorded. Socioeconomic status was determined using the social risk index (SRI),29 as described previously.6 The SRI provides an indication of social and economic status (range 0-12, with 0 indicating highest status) based on 6 key aspects: family structure, highest education completed by primary caregiver, employment status of primary income earner, occupation of primary income earner, language spoken in the home, and maternal age at the birth of the child. Maternal occupation was converted to an occupational status score developed from the Census of 2006.30 This score ranges from 0-100 with a higher score indicative of higher occupational prestige. QOL Assessment The OSA-18, specifically designed to assess QOL associated with SDB, determined health-related QOL (HRQOL).31 The items are scored on a 7-point Likert scale anchored by 1 = none of the time; and 7 = all of the time and grouped into 5 domains: sleep disturbance, physical symptoms, emotional symptoms, daytime functioning, and caregiver concerns. A total score less than 60 suggests the child’s SDB has a small impact on HRQOL, between 60 and 80 indicates a moderate impact, and greater than 80 indicates a large impact. The scores from the individual domains and total score at follow-up were subtracted from the scores at baseline to determine the change score. A negative change score indicates a deterioration of HRQOL, whereas a positive change score indicates an improvement. 1273
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Change scores of <0.5 indicates no change, 0.5-0.9 a small change, 1.0-1.4 a moderate change, and >1.4 a large change.32 General QOL was assessed with the Pediatric Quality of Life Inventory (PedsQL) 4.0 Generic Core Scales ParentReport (henceforth called “child PedsQL”).33 The child PedsQL is a 21-item (aged 2-4 years) or 23-item (aged 512 years) questionnaire that provides 4 functional domains (physical, emotional, social, and school) and 2 summary scales (psychosocial health and total score). Item scores were linearly transformed to a scale of 0-100, with higher scores representing better QOL. Age standardized z-scores were calculated using published normative data.34 Parent HRQOL and family functioning were assessed using the 36-item PedsQL Family Impact Module (henceforth called “family PedsQL”).35 This questionnaire contains 8 subscales (physical, emotional, social and cognitive functioning, communication, worry, daily activities, and family relationships), which are summed to provide a summary score for parent HRQOL, family functioning, and total score. Item scores were transformed as detailed above. Normative data is not available for this module. All questionnaires have been shown to be sensitive to detecting changes following adenotonsillectomy in children with SDB.8,18 Parental Stress Assessment The level of parental stress was assessed using the parenting stress index (PSI), third edition, short form.36 This 36-item self-report questionnaire provides 3 subscales (parental distress, parent-child dysfunction, and difficult child) and a total stress score. An indication of the level of defensive responding is also provided to account for reporter bias. Raw scores were converted to centiles for analysis. Statistical Analyses Statistical analyses were performed using SPSS (IBM Statistics v 20; SPSS Inc, Chicago, Illinois). Data were tested for normality and equal variance. All respiratory variables showed a positive skew and were analyzed using nonparametric analyses. Continuous demographic data were analyzed using repeated measures ANOVA. Categorical data were assessed using c2 analysis. Group differences in PSG recorded sleep variables over time were analyzed with repeated measures ANOVA with Bonferroni post-hoc testing where ANOVA was significant (P < .05). Differences in respiratory variables were assessed using Kruskal-Wallis ANOVA on ranks, with Mann-Whitney U post-hoc testing where appropriate (P < .05). Linear mixed-model analyses were used to determine the fixed effects of time and resolution of SDB on QOL and parental stress outcomes. OAHI was entered as a covariate to determine the predictive value of changes in SDB severity on changes in psychosocial outcomes. Subject was used as the random effect, accounting for interindividual differences. Group differences in the change in scores in the OSA-18 and child PedsQL were analyzed using a 1-way ANOVA. 1274
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Results At follow-up, 19% of the original cohort could not be contacted, 41% declined further participation, and 2 controls were ineligible as they were diagnosed with a behavioral disorder following the baseline study. Reasons for refusal included the original referral issue had resolved and their child did not need a repeat sleep study (49%); the child refused to participate (18%); parent was too busy (12%); parental illness or accident (7%); parent was unhappy with the clinical process at baseline (7%); or the family had moved outside the metropolitan area (7%). Seven percent did not provide a reason for refusal. Final response rate was 30% for the children originally diagnosed with SDB and 68% for the control group. Two control children were subsequently excluded from analysis because of developing SDB. The proportion of children who were treated was not significantly different between the children who returned and those who did not (P = .15). There were no differences in age, sex, body mass index z-score, maternal occupation, or maternal education between those that refused and those that returned. The SRI was higher in those who did not return (mean SD = 1.4 1.7) compared with those who did return (mean SD = 0.8 1.1, P = .016), indicating that those who refused were from a slightly lower socioeconomic background. There were no differences in any of the psychosocial domains at baseline between participating and nonparticipating children with SDB at follow-up. The families of nonsnoring control children scored higher on the domain of cognitive functioning (indicating better functioning) on the family PedsQL questionnaire (t [17.3] = 2.2, P = .037) and scored lower on parental distress (indicated less distress) (t [36] = 2.0, P = .049) at baseline than the nonsnoring controls that did not return. Demographics As can be seen in Figure 1 (available at www.jpeds.com), 29% of children originally diagnosed with primary snoring, 31% with mild OSA, and 33% with MS OSA returned. Of these, 38% of children with primary snoring, 55% with mild OSA and 100% with MS OSA were treated. Of those that were treated, 33% of children with primary snoring, 50% with mild OSA, and 63% with MS OSA resolved. Spontaneous resolution also occurred in 60% of children with primary snoring and 40% with mild OSA. In total, 51% (18/35) of children originally diagnosed with SDB had resolved and 49% (17/35) had ongoing SDB. Furthermore, 90% (18/20) of the treated children underwent surgery for removal of tonsils and/or adenoids, and 10% (2/20, both mild OSA) received medical treatment in the form of nasal steroids (Table I). Sleep and Respiratory Variables All children slept more than 5 hours during the PSG on both the baseline (mean SD = 443 37 minutes) and follow-up (mean SD = 429 47 minutes) studies. Changes in sleep Biggs et al
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Table I. Cohort demographics Control (N = 25) Age (y: mean SD) BMI z-score (mean SD) Sex (N, % male) Maternal education (N, % tertiary educated) Maternal occupation (mean SD, range 0-100) English language exposure (N, % English only) SRI (mean SD)
Resolved (N = 18)
Unresolved (N = 17)
Baseline
Follow-up
Baseline
Follow-up
Baseline
Follow-up
P
4.2 (1.1) 0.5 (1.2)
7.5 (1.1) 0.4 (0.9) 11 (44) 18 (72) 74 (19) 23 (92) 0.4 (0.9)
4.6 (0.8) 0.7 (1.2)
7.8 (0.9) 0.7 (0.8) 15 (83) 7 (39) 58 (17) 11 (61) 1.2 (1.5)
4.2 (0.8) 0.6 (1.0)
7.3 (0.9) 0.3 (1.0) 8 (47) 12 (75) 67 (19) 11 (65) 0.9 (1.1)
NS* NS* .02† .03† .02z NS† .02x
BMI, body mass index; NS, nonsignificant. *Repeated measures ANOVA: significance value of group main effect reported. †c2 analysis. zOne-way ANOVA. xKruskal-Wallis ANOVA on ranks.
variables over time were as expected with increasing age. Overall %N1 (F [1,56] = 10.1, P = .002), % total REM (F [1,56] = 4.9, P = .03), and sleep efficiency (F [1,56] = 6.4, P = .02) decreased over time. Overall %N2 (F [1,56] = 37.1, P < .001), % total NREM (F [1,56] = 5.6, P = .02), and % wake after sleep onset (F [1,56] = 9.4, P = .003) increased over time. At both baseline and follow-up, children in the control group obtained more NREM (F [1,56] = 5.3, P = .008) and less REM (F [1,56] = 5.0, P = .01) than the children in the resolved group. There were no differences in sleep variables between the control and unresolved groups. There were no significant interactions between group and time indicating that there was no effect of resolution of SDB on the change in sleep variables over time. By design, significant differences in OAHI between the control and resolved groups at baseline were no longer evident at follow-up. OAHI remained significantly higher in the unresolved group compared with the control group (Mann-Whitney U = 49.5, P < .001) and became significantly higher than the resolved group (Mann-Whitney U = 44.0, P < .001) at follow-up. This pattern was also observed in the arousal index. Oxygen saturation improved for all groups over time. Psychosocial Outcomes Table II shows the means and 95% CIs for all psychosocial outcome measures. A higher score on both the OSA-18 and PSI indicate poorer psychosocial functioning. Conversely, higher scores on the child and family PedsQL indicate better QOL. OSA-18 The mixed-model analysis revealed a significant effect of group for all HRQOL measures (Table II). Mean scores were significantly higher, indicating poorer HRQOL, in both the resolved and unresolved groups than control for the domains of sleep disturbance, physical symptoms, emotional symptoms, daytime functioning, and caregiver concern. There were no differences between the resolved and unresolved groups. There was a significant improvement of HRQOL sleep disturbance at follow-up
compared with baseline. Post-hoc analysis revealed that the resolved group had significantly greater improvement in sleep disturbance, daytime functioning and caregiver concern than the unresolved group. Analysis of the change scores shows a large change in sleep disturbance, a moderate change in physical symptoms and caregiver concern, and a small, nonsignificant, change in emotional symptoms and daytime functioning in the resolved group compared with the unresolved and control groups (Figure 2, A). A reduction in OAHI significantly predicted an improvement in physical symptoms (b = 0.2, P = .001), but not on any other subscale. PedsQL Overall, scores on the child and family PedsQL remained unchanged between baseline and follow-up (Table II). Post-hoc analyses revealed that for all domains, except family social functioning, there were no differences between the resolved and unresolved groups, however, both groups scored significantly lower (ie, worse general QOL) than the control group. For family social functioning, scores were not different between the control and unresolved groups, with both groups scoring significantly higher (ie, better general QOL) than the resolved group. Figure 2, B shows the change in z-score from baseline to follow-up in the child PedsQL. A change in OAHI was significantly, negatively related to school functioning on the child PedsQL questionnaire, with a decrease in OAHI predicting an increase in school functioning (b = 2.4, P = .026). A change in OAHI was also significantly negatively related to worry and family relationships on the family PedsQL questionnaire, with a decrease in OAHI predicting an improvement in QOL related to family worry (ie, less worry: b = 2.5, P = .043) and family relationships (ie, improved relationships: b = 3.7, P < .01). Parental Stress Mixed model results for the PSI are shown in Table II. Overall levels of parental stress did not change between baseline and follow-up, irrespective of whether SDB had
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Table II. Results of mixed model analysis for OSA-18, PedsQL, and parental stress index Results of mixed model fixed effects Control
OSA-18 Sleep disturbance Physical symptoms Emotional symptoms Daytime functioning Caregiver concern Total score Child PedsQL Physical Emotional Social School Psychosocial health Total Family PedsQL Physical Emotional Social Cognition Communication Worry Daily activities Family relationships Parent health Family summary Total PSI Parental distress Parent-child dysfunction Difficult child Total stress
Resolved
Unresolved
Time
Group
Time group
Baseline
Follow-up
Baseline
Follow-up
Baseline
Follow-up
F
F
F
1.3 (1.2-1.5) 1.6 (1.4-1.8) 2.3 (1.9-2.6) 1.5 (1.3-1.7) 1.2 (1.1-1.3) 27 (25-29)
1.2 (1.0-1.3) 1.3 (1.1-1.4) 1.8 (1.4-2.2) 1.3 (1.1-1.4) 1.2 (1.0-1.5) 24 (21-26)
4.0 (3.4-4.6) 3.5 (2.6-4.3) 3.8 (3.1-4.4) 3.2 (2.7-3.6) 3.6 (2.7-4.5) 66 (56-76)
2.0 (1.4-2.5) 2.3 (1.7-2.8) 3.0 (2.3-3.7) 2.3 (1.6-3.0) 2.3 (1.5-3.1) 41 (32-50)
3.5 (2.9-4.1) 2.8 (2.2-3.3) 3.4 (2.8-4.1) 2.8 (2.2-3.3) 2.8 (2.3-3.4) 54 (47-62)
2.8 (2.3-3.3) 2.8 (2.2-3.4) 3.2 (2.2-4.1) 2.7 (2.3-3.2) 2.7 (2.0-3.3) 50 (42-59)
5.6* 2.1 0.2 2.0 1.1 1.8
45.8†,z 14.1†,z 9.7†,z 30.4†,z 27.1†,z 37.0†,z
10.8† 2.6 1.3 3.4* 4.2* 7.9x
93 (90-96) 87 (83-92) 92 (86-98) 94 (89-98) 91 (87-95) 91 (88-95)
95 (92-98) 83 (76-89) 93 (88-98) 92 (88-95) 89 (85-93) 91 (88-95)
82 (74-91) 66 (58-73) 82 (72-91) 82 (73-91) 75 (69-82) 78 (72-85)
78 (67-89) 67 (55-78) 82 (72-91) 74 (62-85) 74 (65-83) 75 (66-85)
82 (75-89) 64 (54-74) 83 (75-91) 86 (78-94) 77 (70-83) 78 (72-85)
84 (78-89) 65 (53-76) 80 (74-87) 73 (65-80) 72 (66-79) 77 (71-82)
0.2 0.1 2.8 0.7 0.8 0.4
10.4†,{ 12.3†,{ 5.7x,{ 8.3x,{ 13.1†,{ 14.0†,{
0.9 0.7 0.0 0.5 0.1 0.2
93 (90-96) 93 (89-98) 95 (90-99) 96 (93-99) 97 (95-100) 98 (96-99) 92 (85-99) 94 (90-98) 95 (91-97) 95 (92-97) 95 (92-97)
94 (89-98) 93 (88-98) 98 (96-100) 94 (90-98) 99 (97-100) 96 (93-100) 93 (88-99) 95 (90-99) 95 (91-98) 94 (90-99) 95 (92-98)
69 (61-77) 76 (66-85) 78 (70-88) 76 (65-87) 82 (73-91) 70 (57-83) 67 (56-78) 74 (64-85) 74 (66-82) 72 (62-81) 74 (66-81)
75 (64-86) 75 (64-86) 83 (70-96) 78 (65-92) 82 (96-94) 78 (68-88) 69 (55-84) 76 (63-89) 78 (67-88) 74 (61-86) 77 (67-87)
76 (69-84) 79 (71-87) 88 (82-94) 80 (72-89) 84 (76-91) 81 (73-89) 67 (54-81) 75 (63-87) 80 (74-86) 71 (62-85) 78 (72-85)
79 (70-88) 77 (67-87) 86 (74-98) 82 (69-95) 82 (72-92) 82 (73-91) 74 (61-88) 73 (61-86) 81 (71-90) 74 (62-86) 79 (71-88)
2.0 0.4 0.7 0.1 0.1 1.0 0.1 0.2 0.2 0.1 0.1
21.4†,{ 9.4†,{ 8.5x,** 8.0x,{ 10.8†,{ 12.6†,{ 9.0†,{ 7.3x,{ 16.0†,{ 10.0†,{ 18.3†,{
1.4 0.2 0.4 0.7 0.1 0.9 0.9 1.1 0.8 0.9 1.2
42 (28-57) 42 (27-56) 46 (30-61) 40 (37)
19 (9-29) 26 (16-36) 26 (15-38) 19 (26)
43 (27-59) 44 (28-59) 62 (48-77) 57 (33)
35 (19-51) 45 (27-64) 55 (36-75) 48 (36)
42 (25-59) 49 (34-64) 59 (43-75) 49 (35)
48 (33-63) 54 (36-72) 63 (46-80) 62 (31)
1.1 0.0 0.1 0.9
1.3 2.8 7.5†,z 6.0x,††
0.4 0.1 0.2 0.2
F, ratio of between group variance to within group variance. Data for the OSA-18 are presented as raw scores. The linearly transformed score of 0-100 is presented for PedsQL, and centiles are presented for PSI. All data are presented as mean (95% CI). *P < .05. †P < .001. zControl < resolved = unresolved. xP < .01. {Control > resolved = unresolved. **Control > resolved. ††Control < unresolved.
resolved. Post-hoc analyses of group differences showed parents indicated more stress relating to a difficult child in both the resolved and unresolved groups compared with the control group. Parents of children with unresolved SDB reported significantly more total stress than parents of control children. A change in OAHI was significantly, negatively associated with a change in scores for stress related to a difficult child (b = 1.9, P = .048), indicating that an improvement in OAHI was predictive of decreased scores on the difficult child scale (ie, less difficult).
Discussion This study revealed that a reduction in respiratory obstruction, as measured by the OAHI, was associated with an improvement in some aspects of QOL, family functioning, and parental stress, yet complete resolution of SDB did not 1276
normalize these outcomes. With little exception, psychosocial functioning remained poorer in children originally diagnosed with SDB than nonsnoring controls, irrespective of resolution. The OSA-18 showed an improvement in domains specifically relating to SDB severity in children whose SDB had resolved compared with the unresolved group, however, impairments in domains of general functioning such as emotional symptoms and daytime functioning remained. This was also reflected in the PedsQL and parental stress measures, with resolution having no impact on any change in scores from baseline to follow-up on the PedsQL or PSI. The continued psychosocial impairment in children originally diagnosed with SDB in the current study is consistent with behavioral data reported in our previous study of school-aged children.20 This could imply that any insult during early development because of SDB is irreversible. Alternatively, these results support the referral bias theory that states parents of children with mild forms of SDB seek medical investigation because of concomitant behavioral issues rather Biggs et al
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Figure 2. Group differences in A, change in domain scores of the OSA-18 and B, child PedsQL. A positive score indicates an improvement from baseline to follow-up. A negative score indicates poorer functioning. Data are mean and SEs. *P < .05. † P < .01. zP < .001.
than concerns about sleep per se. If behavioral difficulties were the mediator of psychosocial outcomes, resolution of the respiratory symptoms may not result in long-term improvements. Current clinical treatment decisions are based on a number of factors including clinical history, physical examination including the size of the lymphoid tissue, and when available, the metrics assessed by PSG.2 Clinical evidence supports surgical intervention for MS OSA, but if PSG metrics, such as OAHI, sleep fragmentation, and oxygen desaturation, do not show significant OSA, surgical treatment is not usually prescribed, primarily because of the risks involved with the procedure.37 This study supports previous research that has consistently shown these metrics to be poor predictors of behavioral,5,6,38 cognitive,7,39 and psychosocial
dysfunction.10,15 Most recently, the Childhood Adenotonsillectomy Trial showed that although children with OSA (mean Obstructive Respiratory Disturbance Index <8 events/hour) randomized into the early tonsillectomy group, showed improved QOL 7 months after surgery compared with those in the watchful waiting group, these improvements were only minimally explained by changes in PSG variables.15 Combined, these and the current results add to the mounting evidence that alternate assessment variables are needed for children with milder forms of SDB. Despite no difference in psychosocial impairment between the children who resolved and those that did not at followup, this study does show a significant relationship between a reduction in OAHI and outcomes relating to family
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functioning and parental stress. It was recently shown that school-aged children with MS OSA had greater improvement in OSA-18 sleep disturbance, caregiver concern, and total score than those with mild OSA or primary snoring.17 Although that study did not include a posttreatment PSG, rendering it impossible to determine if any of the treated children had residual disease, it does suggest that improvement in psychosocial outcomes are dependent on disease severity. In contrast, the Tucson Children’s Assessment of Sleep Apnea study showed that having persistent SDB from childhood to early adolescence significantly increased the odds of behavioral and adaptive dysfunction.40 In the current study, the greatest reduction in OAHI was observed in children originally diagnosed with MS OSA, irrespective of whether they met our definition for resolution. Treatment, surgical or otherwise, is not routinely recommended for children with primary snoring and is only occasionally recommended for children with mild OSA, unless significant adenotonsillar hypertrophy is present.2 Our data support these current treatment practices, however, as children with milder SDB appear less likely to resolve with treatment, and as those with unresolved SDB continue to experience poor psychosocial outcomes, alternate or additional treatment or interventions for children with mild forms of SDB are required. The primary limitation of this study was the low response rate, with those refusing participation outnumbering those who agreed. Although nonresponders had similar demographic backgrounds, treatment history, and psychosocial outcomes at baseline to responders, selection bias is a possibility. The low response also resulted in the study being underpowered to effectively examine changes in psychosocial functioning by severity and resolution. Finally, we were unable to determine the impact of untreated MS OSA on outcomes as all participants originally diagnosed with MS OSA were treated. Nonetheless, the examination of psychosocial outcomes following complete resolution of SDB rather than simply by treatment is a strength of this study. It is now understood that treatment, surgical or otherwise, does not always result in resolution of SDB both in the short22 and long term.20,21 Although preliminary, by eliminating the confounder of residual disease on long-term outcomes in the analysis, this study provides a greater understanding of the efficacy of treatment and ongoing psychosocial dysfunction in children with SDB. This study shows that children with SDB, irrespective of resolution, continue to experience psychosocial dysfunction over the long term. Future research examining alternate or additional interventions to improve psychosocial outcomes in children with SDB, is an essential next step in this field. n We thank Mark Tacey for his statistical advice. Submitted for publication Apr 29, 2015; last revision received Jul 14, 2015; accepted Sep 3, 2015.
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Vol. 167, No. 6 Reprint requests: Sarah N. Biggs, PhD, The Ritchie Center, Level 5 Monash Medical Center, Level 5, 246 Clayton Rd, Clayton, Victoria 3168, Australia. E-mail: [email protected]
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Figure 1. Flow chart depicting response rate from baseline to follow-up, the proportion of children in each sleep disorder breathing group that were treated, and the proportion of those who were treated that were resolved at follow-up.
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