http://informahealthcare.com/pdr ISSN: 1751-8423 (print), 1751-8431 (electronic) Dev Neurorehabil, 2014; 17(6): 420–425 ! 2014 Informa UK Ltd. DOI: 10.3109/17518423.2014.941116
ORIGINAL ARTICLE
Does hip displacement influence health-related quality of life in children with cerebral palsy? Nikolai H. Jung1, Barbara Pereira1,2, Ina Nehring1,3, Olga Brix4, Peter Bernius5, Sebastian A. Schroeder4, Gerhard J. Kluger6, Tillmann Koehler7, Andreas Beyerlein8, Shannon Weir9, Ru¨diger von Kries3, Unni G. Narayanan9, Steffen Berweck4,6*, & Volker Mall1*
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1
Department of Pediatrics, Technische Universita¨t Mu¨nchen, Munich, Germany, 2Department of Paediatrics and Adolescent Medicine, University Medical Center Freiburg, Freiburg, Germany, 3Ludwig-Maximilians-Universita¨t Mu¨nchen, Institute for Socialpaediatrics and Adolescent Medicine, Munich, Germany, 4Department of Paediatric Neurology and Developmental Medicine, Hauner Children’s Hospital, University of Munich, Munich, Germany, 5Scho¨n Klinik Harlaching, Clinic for Paediatric Orthopaedics, Munich, Germany, 6Scho¨n Klinik Vogtareuth, Clinic for Neuropediatrics and Neurorehabilitation, Vogtareuth, Germany, 7Childrens Center Mecklenburg GmbH, Schwerin, Germany, 8Institute of Diabetes Research, Helmholtz Zentrum Mu¨nchen, Munich, Germany, and Forschergruppe Diabetes der Technischen Universita¨t Mu¨nchen, Munich, Germany, and 9The Hospital for Sick Children, Division of Orthopedic Surgery, Toronto, Ontario, Canada Abstract
Keywords
Objective: To evaluate the association of hip lateralisation with health-related quality of life (HRQL) in children with cerebral palsy (CP) using the Caregiver Priorities and Child Health Index of Life with Disabilities (CPCHILDÕ ) questionnaire. Methods: We assessed n ¼ 34 patients (mean age: 10.2 years, SD: 4.7 years; female: n ¼ 16) with bilateral CP and Gross Motor Function Classification System (GMFCS) Level III–V using the CPCHILDÕ questionnaire. Hip lateralisation was measured by Reimer‘s migration percentage (MP). Results: There was an association between both, MP and GMFCS with CPCHILDÕ total score. Stratified analyses did not suggest interaction of the association between MP and CPCHILDÕ total score by GMFCS level. After adjustment for GMFCS level, we found a significant linear decrease of CPCHILDÕ total score of 0.188 points by 1% increment in MP. Conclusions: There was an association between MP and HRQL, which could not be explained by the GMFCS level.
Cerebral palsy, CPCHILD, health related quality of life, hip displacement, quality of life
Introduction Hip displacement is a common focal motor problem, second only to equinus foot deformity in patients with cerebral palsy (CP) [1]. It is primarily caused by muscle imbalance and may consecutively lead to complete lateralisation and dislocation of the hip [2]. The risk of hip displacement depends on severity of motor impairment measured by the gross motor function classification system (GMFCS) and ranges from 0% in mild impaired (GMFCS level I) up to 90% in severely impaired (GMFCS level V) children [3]. Lateralisation of the hip contributes to impairment in sitting and walking, and may account for painful degenerative arthritis in 40–84% of the patients [4–7]. A European study demonstrated pain to be common in children with CP for different reasons and found it was associated with lower quality of life (QoL) measured by the KIDSCREEN questionnaire [8]. QoL is defined according
*Shared senior authorship. Correspondence: Dr. Med. Nikolai H. Jung, Department of Pediatrics, Technische Universita¨t Mu¨nchen, Kinderzentrum Mu¨nchen gemeinnu¨tzige GmbH, Heiglhofstrasse 63, 81377 Mu¨nchen, Germany. Tel: +49 89 71009 105. Fax: +49 89 71009 148. E-mail: [email protected]
History Received 14 January 2014 Revised 25 June 2014 Accepted 30 June 2014 Published online 24 July 2014
to the WHO as ‘an individual’s perception of their position in life in the context of the culture and value systems in which they live, and in relation to their goals, expectations, standards and concerns’ [9]. Health-related quality of life (HRQL) in particular comprises the health-related aspects of life that contribute towards perception of well-being, and the ability to fulfil and take part in certain life roles. According to the WHO classification of function, disability and health, especially motor impairment, leads to restrictions on the level of participation, which also plays a role in children with CP [10]. Limitations on this level and pain might influence HRQL in patients with CP and hip displacement. To evaluate HRQL in children with CP, the Caregiver Priorities and Child Health Index of Life with Disabilities (CPCHILDÕ ) questionnaire was developed and validated for severely impaired children according to the GMFCS [11, 12]. It consists of seven sections including ratings of activities of daily life, transfer and mobility, comfort, communication and social interaction as well as questions about the general health status and overall QoL. Data from adults suggest that hip lateralisation is associated with lower HRQL [13, 14] because of restrictions in mobility and pain related to the disease. Similarly, it was recently found to be associated with pain and restrictions
Influence of hip displacement on quality of life
DOI: 10.3109/17518423.2014.941116
in mobility in children with CP [4]. Therefore, it is plausible to hypothesise that hip lateralisation might be associated with reduced HRQL in children with CP. In a cross-sectional study, we assessed the association between MP and HRQL in children with severe CP (GMFCS level III–V).
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ordinal scale, from 0 (‘Least important’) to 5 (‘Most important’). Scores for each section/domain and for the total survey (total score) are standardised and range from 0 (worse) to 100 (best). Measurement of hip lateralisation
Methods This study was conducted in accordance with the good clinical practice guidelines and the declaration of Helsinki. It was approved by the local ethics committee (Freiburg, Germany, vote 193/09) and informed written consent of the parents or primary caregivers of the patients and, if possible, of the patients themselves was obtained.
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Participants Primary caregivers (mean age: 40.9 years; SD: 7.9; females ¼ 31) of n ¼ 34 patients aged 2–21 years (mean age: 9.8 years; SD: 4.7; 16 females and 18 males) with bilateral spastic CP (n ¼ 32) and dystonic CP (n ¼ 2) took part in this study. Patients were recruited from the outpatient clinic in Freiburg and Munich (Ludwig-Maximilians University). Severity of motor impairment was categorised according to the GMFCS [15, 16] and was rated by an experienced investigator. GMFCS levels ranged from III to V. Seven patients had level III, n ¼ 15 level IV and n ¼ 12 level V (Table I). Eight patients had prior orthopaedic surgery ranging from preventive to salvage surgery at least 12 months before inclusion in the study. CPCHILDÕ questionnaire Caregivers were asked to rate HRQL via the CPCHILDÕ questionnaire [11, 12]. Prior to the study, the CPCHILDÕ questionnaire was translated into German language with permission and assistance from the creator [12]. It consists of 37 items distributed over six sections representing the following domains: (1) Activities of Daily Living/Personal Care (nine items); (2) Positioning, Transfer, and Mobility (eight items); (3) Comfort and Emotions (nine items); (4) Communication and Social Interaction (seven items); (5) Health (three items); and (6) Overall Quality Of Life (one item). The sections, which involve the performance of skills, the degree of difficulty of accomplishing each task or activity were rated on a seven-point ordinal scale anchored by 6 (‘No problem at all’) to 0 (‘Impossible’). In Section 7 (Importance of Items), caregivers were asked to rate the importance of each of the items (in the questionnaire) contribution to their child’s overall QoL, using a six-point Table I. Proportions of children with MP533% and MP 33% by GMFCS level and age of the respective participants at different GMFCS level. GMFCS III IV V Total
Age median [range] 7.0 9.0 11.0 9.0
[2.0–18.0] [4.0–16.0] [4.0–21.0] [2.0–21.0]
MP533% [n]
MP 33% [n]
3 6 7 16
4 9 5 18
GMFCS: gross motor function classification system; MP: migration percentage.
We used the Reimers’ migration percentage (MP) to evaluate the lateral displacement of the hip [17] which showed excellent reliability [18]. Pelvic radiographs (anterior–posterior direction) were taken and measurements were performed by experienced paediatric radiologists. To determine the lateral margin of the acetabulum, the lateral margin of the sourcil was used. In hips with a ‘Gothic arch’ formation, the medial point of the arch was used as a reference point which corresponds to the lateral margin of the sourcil [19]. The worst MP of the right or left hip was taken for further analyses. Measurement of pain The Faces Pain Scale was used to assess pain independent from the questions of the survey relating to pain and explicitly locate the area of pain [20]. Different types of faces depict a stepwise increment of pain intensities ranging from ‘no pain’ until ‘very much pain’ in five steps. Participants were asked to point to the face that shows how much pain they have. Statistical analysis Multiple linear regression analyses were conducted to determine the association between GMFCS and MP as explanatory variables with CPCHILDÕ total score. For correlation analyses, the Pearson’s correlation coefficient was used for the total score and all subdomains, except the health domain where Spearman’s correlation coefficient was used as data were not normally distributed. The change of CPCHILDÕ total score and section scores by incremental MP (unit: 1%) was estimated from the value in the multivariate linear regression model with adjustment for GMFCS level. The beta value indicates the increment in HRQL (CPCHILDÕ ) by one unit (1%) of increment in MP. Corresponding 95% confidence intervals (95% CI) were calculated. The potential interaction of the association between MP and CPCHILDÕ total score by GMFCS level was assessed by stratified analyses and assessed for interaction. The sample size was sufficient to detect a value of at least 0.22 with an alpha value of 0.05 and a Power of 80%. To test the differences in MP between right and left side, a two-tailed Student’s paired t-test was performed. All values are given as mean ± standard deviation (SD), if not indicated otherwise. Box plots display median, 25th and 75th percentile (boxes) and the 3rd and 97th percentile (whiskers). Outliers are graphically shown as separate points. Analyses were performed using SAS 9.2 for windows or SPSS version 15.0 (SPSS Inc., Chicago, IL).
Results Mean CPCHILDÕ total score in the n ¼ 34 patients was 53.63 SD 11.56 ranging from 34.92 to 78.33. The proportions of
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Dev Neurorehabil, 2014; 17(6): 420–425
children with MP533% and MP 33% by GMFCS level and age of the respective participants at different GMFCS level are depicted in Table I. Mean MP of all patients of the right hip was 32.57% (SD 22.05; 7–100%) and 37.32% (SD 27.51; 7–100%) for the left hip. No significant differences in MP between right and left hip were found (p ¼ 0.248). Mean of the worst MP (right or left hip) was 41.28% (SD 26.38) ranging from 10% to 100%. In Figure 1, a significant linear decrease of CPCHILDÕ total score by incremental MP [%] is depicted (r ¼ 0.382; p ¼ 0.026) with a crude ¼ 0.17 (95% CI:0.319; 0.028). In subdomains, MP correlated well with standardised scores of the Health section (r ¼ 0.571; p50.001; Figure 2A) and Communication and Social Interaction section (r ¼ 0.765; p50.026; Figure 2B). Specific standardised scores were 74.38 (SD 14.64; Health) and 53.88 (SD 23.76; Communication and Social Interaction). All other subdomains revealed no significant correlation. Figure 3 illustrates that total scores of the CPCHILDÕ questionnaire are also related to GMFCS level with a significant decrease in incremental GMFCS levels. We therefore present stratified and adjusted analyses of the association between CPCHILDÕ and incremental MP in Table II. In all strata, a clear decrease in CPCHILDÕ total score by incremental MP was observed. The decrease appeared to be highest in GMFCS level III. Interaction testing however did not confirm a significant higher effect in children with GMFCS III. For subdomains, a significant decrease of CPCHILDÕ scores was found for Communication and Social Interaction section with ¼ 0.37 (95% CI: 0.628; 0.1183) and Health ( ¼ 0.31; 95% CI: 0.4764; 0.1517) but not for other subdomains.
0-5 yrs. 6-11 yrs. 12-17 yrs. ≥18 yrs.
100
80
Totalscore
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60
40
20
r =−0.382
0 0
20
40
60
80
100
Migration percentage
Figure 1. Correlation of single migration percentage data and total score of the CPCHILDÕ . Data correlated significantly using Pearson’s correlation coefficient. Different symbols apply for children at different ages indicating no age effect on the total score.
There was no association of HRQL and pain in a small subsample of n ¼ 18 measured by the faces pain scale with no correlation of hip pain and total score (r ¼ 0.11, p ¼ 0.66) and hip pain and MP (r ¼ 0.12, p ¼ 0.6). In Figure 2(C), a decrease of CPCHILDÕ total score by incremental MP [%] is depicted (r ¼ 0.426; p ¼ 0.078) with a crude ¼ 0.22 (p ¼ 0.08). Adjustment for pain revealed no change with a ¼ 0.23 (p ¼ 0.07).
Discussion In our study on 34 children with CP and GMFCS levels III–V, we demonstrated a decrease in HRQL measured by the CPCHILDÕ questionnaire by incremental MP which was independent of the GMFCS level. The strength of the association appeared to be highest in children with GMFCS level III. The interaction term as an indicator of direct relation of GMFCS level and MP, however, did not confirm significant effect modification indicating MP to affect health-related quality independently from GMFCS level. Hip displacement in children with CP is known to be associated with contractures resulting in pain [4], gross motor function impairment affecting the ability to sit or stand and walk [21], and has consequently been discussed to be linked to impaired QoL [14]. Indeed, recent studies found positive relationships between the child’s comfort level and the ease of mobility [14]. However, the impact of hip displacement on HRQL and its related factors in detail remain unclear so far. Decreased HRQL measured by the CPCHILDÕ total score was not related to pain in a small sub-sample of this study. The main finding of this study is a correlation of hip lateralisation – with higher MP’s associated with lower CPCHILDÕ total scores. Although, incremental motor impairment (GMFCS level) was also associated with decreasing HRQL as reported elsewhere [3, 22], the association between MP and CPCHILDÕ total score remains significant after adjustment for GMFCS. This demonstrates not only an association of HRQL with GMFCS that has been previously reported [11] but also a potential influence of MP on HRQL that has not been demonstrated so far. The fact that the association appeared to be highest in GMFCS level III may account for a more evident functional impairment of ambulatory patients with higher degrees of hip displacement. The association between hip displacement and HRQL was mainly driven by the subdomains communication and social interaction, and the overall health status. The subdomain health status asks for hospitalisation, drug intake and general health. An association between MP and overall health status appears plausible because hip displacement may be related to hospitalisation, intake in analgesics and general health related to care. Communication and Social Interaction does not only address verbal communication but also participation related to the child’s ability for social interaction. Since social interaction in children relates to individual mobility [23], this association appears plausible as well. In addition, hip status of children with CP has been demonstrated to be linked to the rating of general health by the CPCHILDÕ [14]. Despite the fact that the health, and the communication and social interaction domain revealed a significant association with MP, which may be due to the general health status and to
Influence of hip displacement on quality of life
DOI: 10.3109/17518423.2014.941116
(A)
0-5 yrs. 6-11 yrs. 12-17 yrs. ≥18 yrs.
100
60
40
80
60
40
20
r =−0.571
0 0
20
40 60 Migration percentage (C)
80
r=−0.765
0
100
0
20
40 60 Migration percentage
80
100
0 2 Pain 6 score 8
100
80
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0-5 yrs. 6-11 yrs. 12-17 yrs. ≥18 yrs.
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Communication/social interaction section score
Health section score
80
(B)
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60
40
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r =−0.426
0 0
20
40
60
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Migration percentage
Figure 2. (A) Correlation of single migration percentage data with the Health section score and (B) of the Communication and Social Interaction section score of the CPCHILDÕ . (C) In a small subsample of n ¼ 18 where pain was rated on the faces pain scale, a decrease of the total score with incremental MP was observed as well. Different symbols apply for children at different ages (A, B) and for different ratings of pain (C). No age effect for both subdomains was observed.
participation, the significant overall effect is unlikely due to chance. Exclusion of specific questions relying on communication abilities and of the health domain yielded no contribution to the overall effect on total score of the survey. The strength of this study is the use of a standardised and well-validated instrument to evaluate HRQL in children with CP which provides an objective measurement [11]. The German translation of the questionnaire has been validated for children at the age of 2 years and older [12]. Including younger children did not bias the results since confinement of the analysis of children 56 years yielded almost identical associations. As a limiting factor, the relatively small sample size may account for non-significant results in some strata. The sample size however was sufficient to detect a beta of
at least 0.22. The observed effect size was in the expected range. Thus, significant results were obtained. It should also be considered that we did not evaluate supplementary co-variates that may influence HRQL in children with CP in detail such as other CP-related co-morbidities. However, the main focus was on the association between hip displacement and HRQL. Larger sample size studies may answer contributions of other factors in association with hip status. In addition, these studies may specifically rely on differences in therapeutic interventions of hip displacement in children with CP. Although, surgery is likely to influence the lateralisation [24], an independent effect of surgery on HRQL in our sample is highly unlikely since HRQL was performed at least 12 months after surgery with a mean time of 6.3 years
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CPCHILD total score
80
60
40
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0 IV
III
V
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GMFCS level
Figure 3. Box plots of the total score of the CPCHILDÕ questionnaire plotted by GMFCS level displaying a decrease of total scores by incremental GMFCS levels. Box plots display median, 25th and 75th percentile (boxes) and the 3rd and 97th percentile (whiskers). Circles represent outliers. Table II. Linear regression model: CPCHILD total score by MP (%); stratified by GMFCS. GMFCS
n
b
3 4 5 Overall (adjusted for GMFCS and age)
7 15 12 34
0.333 0.148 0.147 0.188
95% CI 0.59; 0.41; 0.34; 0.32;
0.076 0.11 0.04 0.058
(median: 5.5 years.; range: 1–13 years) in our sample. One participant underwent surgery at the minimum of 12 months before study participation. We assessed the association of MP at the time of interview and not that prior to surgery. We additionally assessed whether surgery might account for effect modification in stratified analyses and modelling revealing that there was no effect modification. CPCHILDÕ addresses and evaluates clinical relevant problems in children with CP [14]. Therefore, decrease in CPCHILDÕ total score by MP points towards the importance of hip displacement for HRQL in children with CP. It may be considered a potential outcome measure in studies evaluating different therapeutic interventions and their effectiveness regarding HRQL.
Acknowledgements The authors would like to thank all participating patients and their families.
Declaration of interest The authors report no declarations of interest. The authors alone are responsible for the content and writing of this paper. No special funding was obtained for this study.
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2. Shore B, Spence D, Graham H. The role for hip surveillance in children with cerebral palsy. Current Reviews in Musculoskeletal Medicine 2012;5:126–134. 3. Soo B, Howard JJ, Boyd RN, Reid SM, Lanigan A, Wolfe R, Reddihough D, Graham HK. Hip displacement in cerebral palsy. The Journal of Bone and Joint Surgery American 2006;88: 121–129. 4. Maslon A, Jozwiak M, Pawlak M, Modrzewski T, Grzegorzewski A. Hip joint pain in spastic dislocation: Aetiological aspects. Developmental Medicine and Child Neurology 2011;53:1019–1023. 5. Krebs A, Strobl WM, Grill F. Neurogenic hip dislocation in cerebral palsy: Quality of life and results after hip reconstruction. Journal of Children’s Orthopaedics 2008;2:125–131. 6. Penner M, Xie WY, Binepal N, Switzer L, Fehlings D. Characteristics of pain in children and youth with cerebral palsy. Pediatrics 2013;132:e407–e413. 7. Jozwiak M, Harasymczuk P, Koch A, Kotwicki T. Incidence and risk factors of hip joint pain in children with severe cerebral palsy. Disability and Rehabilitation 2011;33:1367–1372. 8. Dickinson HO, Parkinson KN, Ravens-Sieberer U, Schirripa G, Thyen U, Arnaud C, Beckung E, Fauconnier J, McManus V, Michelsen SI, et al. Self-reported quality of life of 8–12-year-old children with cerebral palsy: A cross-sectional European study. Lancet 2007;369:2171–2178. 9. The World Health Organization Quality of Life assessment (WHOQOL): position paper from the World Health Organization. Social Science & Medicine 1995;41:1403–1409. 10. Michelsen SI, Flachs EM, Uldall P, Eriksen EL, McManus V, Parkes J, Parkinson KN, Thyen U, Arnaud C, Beckung E, et al. Frequency of participation of 8–12-year-old children with cerebral palsy: A multi-centre cross-sectional European study. European Journal of Paediatric Neurology 2009;13:165–177. 11. Narayanan UG, Fehlings D, Weir S, Knights S, Kiran S, Campbell K. Initial development and validation of the Caregiver Priorities and Child Health Index of Life with Disabilities (CPCHILD). Developmental Medicine and Child Neurology 2006;48:804–812. 12. Jung NH, Brix O, Bernius P, Schroeder AS, Kluger GJ, Beyerlein A, Weir S, von Kries R, Narayanan UG, Mall V, Berweck S. German translation of the caregiver priorities and child health index of life with disabilities questionnaire: Test-retest reliability and correlation with gross motor function in children with cerebral palsy. Neuropediatrics 2014. Apr 3 [Epub ahead of print]. 13. Liptak GS. Health and well being of adults with cerebral palsy. Current Opinion in Neurology 2008;21:136–142. 14. Zarrinkalam R, Rice J, Brook P, Russo RN. Hip displacement and overall function in severe cerebral palsy. Journal of Pediatric Rehabilitation Medicine 2011;4:197–203. 15. Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Developmental Medicine and Child Neurology 1997;39:214–223. 16. Morris C. Development of the gross motor function classification system (1997). Developmental Medicine and Child Neurology 2008;50:5. 17. Reimers J. The stability of the hip in children: A radiological study of the results of muscle surgery in cerebral palsy. Acta Orthopaedica Scandinavica Supplementum 1980;184:1–100. 18. Pons C, Remy-Neris O, Medee B, Brochard S. Validity and reliability of radiological methods to assess proximal hip geometry in children with cerebral palsy: A systematic review. Developmental Medicine and Child Neurology 2013;55: 1089–1102. 19. Kim HT, Kim JI, Yoo CI. Diagnosing childhood acetabular dysplasia using the lateral margin of the sourcil. Journal of Pediatric Orthopedics 2000;20:709–717. 20. Bieri D, Reeve RA, Champion GD, Addicoat L, Ziegler JB. The Faces Pain Scale for the self-assessment of the severity of pain experienced by children: Development, initial validation, and preliminary investigation for ratio scale properties. Pain 1990;41: 139–150. 21. Kentish M, Wynter M, Snape N, Boyd R. Five-year outcome of state-wide hip surveillance of children and adolescents with
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cerebral palsy. Journal of Pediatric Rehabilitation Medicine 2011;4: 205–217. 22. Hagglund G, Lauge-Pedersen H, Wagner P. Characteristics of children with hip displacement in cerebral palsy. BMC Musculoskeletal Disorders 2007;8:101. 23. Colver A, Thyen U, Arnaud C, Beckung E, Fauconnier J, Marcelli M, McManus V, Michelsen SI, Parkes J, Parkinson K, Dickinson HO. Association between participation in life situations of children with cerebral palsy and their physical, social, and
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ORIGINAL ARTICLE
Does hip displacement influence health-related quality of life in children with cerebral palsy? Nikolai H. Jung1, Barbara Pereira1,2, Ina Nehring1,3, Olga Brix4, Peter Bernius5, Sebastian A. Schroeder4, Gerhard J. Kluger6, Tillmann Koehler7, Andreas Beyerlein8, Shannon Weir9, Ru¨diger von Kries3, Unni G. Narayanan9, Steffen Berweck4,6*, & Volker Mall1*
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1
Department of Pediatrics, Technische Universita¨t Mu¨nchen, Munich, Germany, 2Department of Paediatrics and Adolescent Medicine, University Medical Center Freiburg, Freiburg, Germany, 3Ludwig-Maximilians-Universita¨t Mu¨nchen, Institute for Socialpaediatrics and Adolescent Medicine, Munich, Germany, 4Department of Paediatric Neurology and Developmental Medicine, Hauner Children’s Hospital, University of Munich, Munich, Germany, 5Scho¨n Klinik Harlaching, Clinic for Paediatric Orthopaedics, Munich, Germany, 6Scho¨n Klinik Vogtareuth, Clinic for Neuropediatrics and Neurorehabilitation, Vogtareuth, Germany, 7Childrens Center Mecklenburg GmbH, Schwerin, Germany, 8Institute of Diabetes Research, Helmholtz Zentrum Mu¨nchen, Munich, Germany, and Forschergruppe Diabetes der Technischen Universita¨t Mu¨nchen, Munich, Germany, and 9The Hospital for Sick Children, Division of Orthopedic Surgery, Toronto, Ontario, Canada Abstract
Keywords
Objective: To evaluate the association of hip lateralisation with health-related quality of life (HRQL) in children with cerebral palsy (CP) using the Caregiver Priorities and Child Health Index of Life with Disabilities (CPCHILDÕ ) questionnaire. Methods: We assessed n ¼ 34 patients (mean age: 10.2 years, SD: 4.7 years; female: n ¼ 16) with bilateral CP and Gross Motor Function Classification System (GMFCS) Level III–V using the CPCHILDÕ questionnaire. Hip lateralisation was measured by Reimer‘s migration percentage (MP). Results: There was an association between both, MP and GMFCS with CPCHILDÕ total score. Stratified analyses did not suggest interaction of the association between MP and CPCHILDÕ total score by GMFCS level. After adjustment for GMFCS level, we found a significant linear decrease of CPCHILDÕ total score of 0.188 points by 1% increment in MP. Conclusions: There was an association between MP and HRQL, which could not be explained by the GMFCS level.
Cerebral palsy, CPCHILD, health related quality of life, hip displacement, quality of life
Introduction Hip displacement is a common focal motor problem, second only to equinus foot deformity in patients with cerebral palsy (CP) [1]. It is primarily caused by muscle imbalance and may consecutively lead to complete lateralisation and dislocation of the hip [2]. The risk of hip displacement depends on severity of motor impairment measured by the gross motor function classification system (GMFCS) and ranges from 0% in mild impaired (GMFCS level I) up to 90% in severely impaired (GMFCS level V) children [3]. Lateralisation of the hip contributes to impairment in sitting and walking, and may account for painful degenerative arthritis in 40–84% of the patients [4–7]. A European study demonstrated pain to be common in children with CP for different reasons and found it was associated with lower quality of life (QoL) measured by the KIDSCREEN questionnaire [8]. QoL is defined according
*Shared senior authorship. Correspondence: Dr. Med. Nikolai H. Jung, Department of Pediatrics, Technische Universita¨t Mu¨nchen, Kinderzentrum Mu¨nchen gemeinnu¨tzige GmbH, Heiglhofstrasse 63, 81377 Mu¨nchen, Germany. Tel: +49 89 71009 105. Fax: +49 89 71009 148. E-mail: [email protected]
History Received 14 January 2014 Revised 25 June 2014 Accepted 30 June 2014 Published online 24 July 2014
to the WHO as ‘an individual’s perception of their position in life in the context of the culture and value systems in which they live, and in relation to their goals, expectations, standards and concerns’ [9]. Health-related quality of life (HRQL) in particular comprises the health-related aspects of life that contribute towards perception of well-being, and the ability to fulfil and take part in certain life roles. According to the WHO classification of function, disability and health, especially motor impairment, leads to restrictions on the level of participation, which also plays a role in children with CP [10]. Limitations on this level and pain might influence HRQL in patients with CP and hip displacement. To evaluate HRQL in children with CP, the Caregiver Priorities and Child Health Index of Life with Disabilities (CPCHILDÕ ) questionnaire was developed and validated for severely impaired children according to the GMFCS [11, 12]. It consists of seven sections including ratings of activities of daily life, transfer and mobility, comfort, communication and social interaction as well as questions about the general health status and overall QoL. Data from adults suggest that hip lateralisation is associated with lower HRQL [13, 14] because of restrictions in mobility and pain related to the disease. Similarly, it was recently found to be associated with pain and restrictions
Influence of hip displacement on quality of life
DOI: 10.3109/17518423.2014.941116
in mobility in children with CP [4]. Therefore, it is plausible to hypothesise that hip lateralisation might be associated with reduced HRQL in children with CP. In a cross-sectional study, we assessed the association between MP and HRQL in children with severe CP (GMFCS level III–V).
421
ordinal scale, from 0 (‘Least important’) to 5 (‘Most important’). Scores for each section/domain and for the total survey (total score) are standardised and range from 0 (worse) to 100 (best). Measurement of hip lateralisation
Methods This study was conducted in accordance with the good clinical practice guidelines and the declaration of Helsinki. It was approved by the local ethics committee (Freiburg, Germany, vote 193/09) and informed written consent of the parents or primary caregivers of the patients and, if possible, of the patients themselves was obtained.
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Participants Primary caregivers (mean age: 40.9 years; SD: 7.9; females ¼ 31) of n ¼ 34 patients aged 2–21 years (mean age: 9.8 years; SD: 4.7; 16 females and 18 males) with bilateral spastic CP (n ¼ 32) and dystonic CP (n ¼ 2) took part in this study. Patients were recruited from the outpatient clinic in Freiburg and Munich (Ludwig-Maximilians University). Severity of motor impairment was categorised according to the GMFCS [15, 16] and was rated by an experienced investigator. GMFCS levels ranged from III to V. Seven patients had level III, n ¼ 15 level IV and n ¼ 12 level V (Table I). Eight patients had prior orthopaedic surgery ranging from preventive to salvage surgery at least 12 months before inclusion in the study. CPCHILDÕ questionnaire Caregivers were asked to rate HRQL via the CPCHILDÕ questionnaire [11, 12]. Prior to the study, the CPCHILDÕ questionnaire was translated into German language with permission and assistance from the creator [12]. It consists of 37 items distributed over six sections representing the following domains: (1) Activities of Daily Living/Personal Care (nine items); (2) Positioning, Transfer, and Mobility (eight items); (3) Comfort and Emotions (nine items); (4) Communication and Social Interaction (seven items); (5) Health (three items); and (6) Overall Quality Of Life (one item). The sections, which involve the performance of skills, the degree of difficulty of accomplishing each task or activity were rated on a seven-point ordinal scale anchored by 6 (‘No problem at all’) to 0 (‘Impossible’). In Section 7 (Importance of Items), caregivers were asked to rate the importance of each of the items (in the questionnaire) contribution to their child’s overall QoL, using a six-point Table I. Proportions of children with MP533% and MP 33% by GMFCS level and age of the respective participants at different GMFCS level. GMFCS III IV V Total
Age median [range] 7.0 9.0 11.0 9.0
[2.0–18.0] [4.0–16.0] [4.0–21.0] [2.0–21.0]
MP533% [n]
MP 33% [n]
3 6 7 16
4 9 5 18
GMFCS: gross motor function classification system; MP: migration percentage.
We used the Reimers’ migration percentage (MP) to evaluate the lateral displacement of the hip [17] which showed excellent reliability [18]. Pelvic radiographs (anterior–posterior direction) were taken and measurements were performed by experienced paediatric radiologists. To determine the lateral margin of the acetabulum, the lateral margin of the sourcil was used. In hips with a ‘Gothic arch’ formation, the medial point of the arch was used as a reference point which corresponds to the lateral margin of the sourcil [19]. The worst MP of the right or left hip was taken for further analyses. Measurement of pain The Faces Pain Scale was used to assess pain independent from the questions of the survey relating to pain and explicitly locate the area of pain [20]. Different types of faces depict a stepwise increment of pain intensities ranging from ‘no pain’ until ‘very much pain’ in five steps. Participants were asked to point to the face that shows how much pain they have. Statistical analysis Multiple linear regression analyses were conducted to determine the association between GMFCS and MP as explanatory variables with CPCHILDÕ total score. For correlation analyses, the Pearson’s correlation coefficient was used for the total score and all subdomains, except the health domain where Spearman’s correlation coefficient was used as data were not normally distributed. The change of CPCHILDÕ total score and section scores by incremental MP (unit: 1%) was estimated from the value in the multivariate linear regression model with adjustment for GMFCS level. The beta value indicates the increment in HRQL (CPCHILDÕ ) by one unit (1%) of increment in MP. Corresponding 95% confidence intervals (95% CI) were calculated. The potential interaction of the association between MP and CPCHILDÕ total score by GMFCS level was assessed by stratified analyses and assessed for interaction. The sample size was sufficient to detect a value of at least 0.22 with an alpha value of 0.05 and a Power of 80%. To test the differences in MP between right and left side, a two-tailed Student’s paired t-test was performed. All values are given as mean ± standard deviation (SD), if not indicated otherwise. Box plots display median, 25th and 75th percentile (boxes) and the 3rd and 97th percentile (whiskers). Outliers are graphically shown as separate points. Analyses were performed using SAS 9.2 for windows or SPSS version 15.0 (SPSS Inc., Chicago, IL).
Results Mean CPCHILDÕ total score in the n ¼ 34 patients was 53.63 SD 11.56 ranging from 34.92 to 78.33. The proportions of
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children with MP533% and MP 33% by GMFCS level and age of the respective participants at different GMFCS level are depicted in Table I. Mean MP of all patients of the right hip was 32.57% (SD 22.05; 7–100%) and 37.32% (SD 27.51; 7–100%) for the left hip. No significant differences in MP between right and left hip were found (p ¼ 0.248). Mean of the worst MP (right or left hip) was 41.28% (SD 26.38) ranging from 10% to 100%. In Figure 1, a significant linear decrease of CPCHILDÕ total score by incremental MP [%] is depicted (r ¼ 0.382; p ¼ 0.026) with a crude ¼ 0.17 (95% CI:0.319; 0.028). In subdomains, MP correlated well with standardised scores of the Health section (r ¼ 0.571; p50.001; Figure 2A) and Communication and Social Interaction section (r ¼ 0.765; p50.026; Figure 2B). Specific standardised scores were 74.38 (SD 14.64; Health) and 53.88 (SD 23.76; Communication and Social Interaction). All other subdomains revealed no significant correlation. Figure 3 illustrates that total scores of the CPCHILDÕ questionnaire are also related to GMFCS level with a significant decrease in incremental GMFCS levels. We therefore present stratified and adjusted analyses of the association between CPCHILDÕ and incremental MP in Table II. In all strata, a clear decrease in CPCHILDÕ total score by incremental MP was observed. The decrease appeared to be highest in GMFCS level III. Interaction testing however did not confirm a significant higher effect in children with GMFCS III. For subdomains, a significant decrease of CPCHILDÕ scores was found for Communication and Social Interaction section with ¼ 0.37 (95% CI: 0.628; 0.1183) and Health ( ¼ 0.31; 95% CI: 0.4764; 0.1517) but not for other subdomains.
0-5 yrs. 6-11 yrs. 12-17 yrs. ≥18 yrs.
100
80
Totalscore
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422
60
40
20
r =−0.382
0 0
20
40
60
80
100
Migration percentage
Figure 1. Correlation of single migration percentage data and total score of the CPCHILDÕ . Data correlated significantly using Pearson’s correlation coefficient. Different symbols apply for children at different ages indicating no age effect on the total score.
There was no association of HRQL and pain in a small subsample of n ¼ 18 measured by the faces pain scale with no correlation of hip pain and total score (r ¼ 0.11, p ¼ 0.66) and hip pain and MP (r ¼ 0.12, p ¼ 0.6). In Figure 2(C), a decrease of CPCHILDÕ total score by incremental MP [%] is depicted (r ¼ 0.426; p ¼ 0.078) with a crude ¼ 0.22 (p ¼ 0.08). Adjustment for pain revealed no change with a ¼ 0.23 (p ¼ 0.07).
Discussion In our study on 34 children with CP and GMFCS levels III–V, we demonstrated a decrease in HRQL measured by the CPCHILDÕ questionnaire by incremental MP which was independent of the GMFCS level. The strength of the association appeared to be highest in children with GMFCS level III. The interaction term as an indicator of direct relation of GMFCS level and MP, however, did not confirm significant effect modification indicating MP to affect health-related quality independently from GMFCS level. Hip displacement in children with CP is known to be associated with contractures resulting in pain [4], gross motor function impairment affecting the ability to sit or stand and walk [21], and has consequently been discussed to be linked to impaired QoL [14]. Indeed, recent studies found positive relationships between the child’s comfort level and the ease of mobility [14]. However, the impact of hip displacement on HRQL and its related factors in detail remain unclear so far. Decreased HRQL measured by the CPCHILDÕ total score was not related to pain in a small sub-sample of this study. The main finding of this study is a correlation of hip lateralisation – with higher MP’s associated with lower CPCHILDÕ total scores. Although, incremental motor impairment (GMFCS level) was also associated with decreasing HRQL as reported elsewhere [3, 22], the association between MP and CPCHILDÕ total score remains significant after adjustment for GMFCS. This demonstrates not only an association of HRQL with GMFCS that has been previously reported [11] but also a potential influence of MP on HRQL that has not been demonstrated so far. The fact that the association appeared to be highest in GMFCS level III may account for a more evident functional impairment of ambulatory patients with higher degrees of hip displacement. The association between hip displacement and HRQL was mainly driven by the subdomains communication and social interaction, and the overall health status. The subdomain health status asks for hospitalisation, drug intake and general health. An association between MP and overall health status appears plausible because hip displacement may be related to hospitalisation, intake in analgesics and general health related to care. Communication and Social Interaction does not only address verbal communication but also participation related to the child’s ability for social interaction. Since social interaction in children relates to individual mobility [23], this association appears plausible as well. In addition, hip status of children with CP has been demonstrated to be linked to the rating of general health by the CPCHILDÕ [14]. Despite the fact that the health, and the communication and social interaction domain revealed a significant association with MP, which may be due to the general health status and to
Influence of hip displacement on quality of life
DOI: 10.3109/17518423.2014.941116
(A)
0-5 yrs. 6-11 yrs. 12-17 yrs. ≥18 yrs.
100
60
40
80
60
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20
r =−0.571
0 0
20
40 60 Migration percentage (C)
80
r=−0.765
0
100
0
20
40 60 Migration percentage
80
100
0 2 Pain 6 score 8
100
80
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20
0-5 yrs. 6-11 yrs. 12-17 yrs. ≥18 yrs.
100
Communication/social interaction section score
Health section score
80
(B)
423
60
40
20
r =−0.426
0 0
20
40
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Migration percentage
Figure 2. (A) Correlation of single migration percentage data with the Health section score and (B) of the Communication and Social Interaction section score of the CPCHILDÕ . (C) In a small subsample of n ¼ 18 where pain was rated on the faces pain scale, a decrease of the total score with incremental MP was observed as well. Different symbols apply for children at different ages (A, B) and for different ratings of pain (C). No age effect for both subdomains was observed.
participation, the significant overall effect is unlikely due to chance. Exclusion of specific questions relying on communication abilities and of the health domain yielded no contribution to the overall effect on total score of the survey. The strength of this study is the use of a standardised and well-validated instrument to evaluate HRQL in children with CP which provides an objective measurement [11]. The German translation of the questionnaire has been validated for children at the age of 2 years and older [12]. Including younger children did not bias the results since confinement of the analysis of children 56 years yielded almost identical associations. As a limiting factor, the relatively small sample size may account for non-significant results in some strata. The sample size however was sufficient to detect a beta of
at least 0.22. The observed effect size was in the expected range. Thus, significant results were obtained. It should also be considered that we did not evaluate supplementary co-variates that may influence HRQL in children with CP in detail such as other CP-related co-morbidities. However, the main focus was on the association between hip displacement and HRQL. Larger sample size studies may answer contributions of other factors in association with hip status. In addition, these studies may specifically rely on differences in therapeutic interventions of hip displacement in children with CP. Although, surgery is likely to influence the lateralisation [24], an independent effect of surgery on HRQL in our sample is highly unlikely since HRQL was performed at least 12 months after surgery with a mean time of 6.3 years
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100
CPCHILD total score
80
60
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0 IV
III
V
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GMFCS level
Figure 3. Box plots of the total score of the CPCHILDÕ questionnaire plotted by GMFCS level displaying a decrease of total scores by incremental GMFCS levels. Box plots display median, 25th and 75th percentile (boxes) and the 3rd and 97th percentile (whiskers). Circles represent outliers. Table II. Linear regression model: CPCHILD total score by MP (%); stratified by GMFCS. GMFCS
n
b
3 4 5 Overall (adjusted for GMFCS and age)
7 15 12 34
0.333 0.148 0.147 0.188
95% CI 0.59; 0.41; 0.34; 0.32;
0.076 0.11 0.04 0.058
(median: 5.5 years.; range: 1–13 years) in our sample. One participant underwent surgery at the minimum of 12 months before study participation. We assessed the association of MP at the time of interview and not that prior to surgery. We additionally assessed whether surgery might account for effect modification in stratified analyses and modelling revealing that there was no effect modification. CPCHILDÕ addresses and evaluates clinical relevant problems in children with CP [14]. Therefore, decrease in CPCHILDÕ total score by MP points towards the importance of hip displacement for HRQL in children with CP. It may be considered a potential outcome measure in studies evaluating different therapeutic interventions and their effectiveness regarding HRQL.
Acknowledgements The authors would like to thank all participating patients and their families.
Declaration of interest The authors report no declarations of interest. The authors alone are responsible for the content and writing of this paper. No special funding was obtained for this study.
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