Bone age in cerebral palsy

Abstracts

OBJETIVOS: Determinar a idade óssea nos pacientes com paralisia cerebral (PC) espástica acompanhados no Ambulatório de Doenças Neuromusculares e comparar com a idade cronológica e correlacionar com os diferentes tipos (hemiparético, diparético, tetraparético), sexo e função motora. MÉTODOS: Analisados 401 pacientes com PC espástica, com idade entre três meses e 20 anos, submetidos a radiografias das mãos e punhos bilaterais e anotado a idade óssea por dois observadores independentes de acordo com o Atlas Greulich & Pyle. RESULTADOS: Quanto a distribuição topográfica, houve um atraso significante (p<0,005) nos tetraparéticos (17,7meses), nos hemiparéticos (10,1 meses) e diparéticos (7,9 meses). No grupo de hemiparéticos, a idade óssea média no lado acometido foi de 96,88 meses e no lado não acometido de 101,13 meses (p<0,005). Em relação ao estado funcional, os não deambuladores demonstraram atraso na idade óssea em relação à idade cronológica de 18,73 meses (p<0,005). Observou-se um maior atraso no sexo masculino (13,59 meses) do que no sexo feminino (9,63 meses), mas não estatisticamente significante (p=0,54). CONCLUSÕES: Há um atraso da idade óssea em relação à idade cronológica influenciado pelo tipo de topografia da espasticidade, nível funcional e sexo na PC. Nível de Evidência IV, Série de Casos.

Paralisia cerebral; Idade óssea; Idade

ORIGINAL ARTICLE

Bone age in cerebral palsy

Eduardo Régis de Alencar Bona Miranda; Maurício D'arc Palmieri; Rodrigo Montezuma César de Assumpção; Helder Henzo Yamada, Daniela Regina Rancan; Patrícia Maria de Moraes Barros Fucs

Faculdade de Ciências Médicas da Santa Casa de São Paulo - São Paulo, SP, Brazil

^{Correspondence}

ABSTRACT

OBJECTIVE: To compare the chronological age and bone age among cerebral palsy patients in the outpatient clinic and its correlation with the type of neurological involvement, gender and functional status.

METHODS: 401 patients with spastic cerebral palsy, and ages ranging from three months to 20 years old, submitted to radiological examination for bone age and analyzed by two independent observers according Greulich & Pyle.

RESULTS: In the topographic distribution, there was a significant delay (p<0.005) in tetraparetic (17.7 months), hemiparetic (10.1 months), and diparetic patients (7.9 months). In the hemiparetic group, the mean bone age in the affected side was 96.88 months and the uncompromised side was 101.13 months (p<0.005). Regarding functional status, the ambulatory group showed a delay of 18.73 months in bone age (p<0.005). Comparing bone age between genders, it was observed a greater delay in males (13.59 months) than in females (9.63 months), but not statistically significant (p = 0.54).

CONCLUSION: There is a delay in bone age compared to chronological age influenced by the topography of spasticity, functional level and gender in patients with cerebral palsy. Level of Evidence IV, Case Series.

Keywords: Cerebral palsy. Bone age. Age.

INTRODUCTION

Cerebral palsy (CP) is a group of non-progressive movement and posture motor disorders resulting from an immature brain injury.^1,2 Brain damage may occur in the pre-natal, birth and post-natal periods. The main damage in CP is the motor impairment and may be associated with other lesions of the central nervous system (CNS) presenting seizures, mental retardation, sensory disorders, speech, hearing and swallowing difficulties, and others. By having multiple disabilities, CP patients require a multidisciplinary approach.^2,3

The motor impairment can be expressed clinically with spasticity, presence of involuntary movements, changes in cerebellar pathways, tremors and stiffness.²

Patients with spastic CP can also be categorized according to the topographical location in tetraparetic, diparetic and hemiparetic. Functionally they can be classified as community-ambulating, home-ambulating, physiotherapy-ambulating and not-ambulating.⁴ They can also be classified according to GMFCS (The Gross Motor Function Classification System) based on the ability to move with an emphasis on walking, sitting and mobility subdivided into five groups, as proposed by Palisano et al.⁵ it should also be taken into account, besides the severity of the disease, also other factors that contribute to the functional level of the patient, such as motivation, presence of deformities, access to the use of orthoses, etc.²

A child with CP often has a weight and height growth deficit, and the main responsible variables can be divided into nutritional and non-nutritional (or neurological) factors.^6,7

Regarding nutritional factors, the inadequate intake of protein can be cited as one of the main causes,⁸ as high energy demand, besides the presentation of motor difficulty in swallowing foods.⁹ On the other hand, non-nutritional factors can be subdivided into direct pathway (negative neurotrophic effect) and indirect (endocrine system, immobility, lack of cargo, etc.).⁸

The orthopedic surgery approach should aim at prevention of skeletal deformities or their correction, but in order to do so, it is important to know the growth abnormalities in children with CP, establishing and taking into account their real bone age, which may not correspond to their chronological age.

Previous studies have proven that there is a delay in bone age in children with CP, even when comparing the affected and unaffected sides of patients with hemiparetic CP.^6,7,9

Our goal is to determine bone age of patients with spastic CP according to Greulich and Pyle¹⁰ and compare them with the chronological age, correlated with the effects of different topographies of spastic CP (tetraparetic, hemiparetic and diparetic), with the influence of functional capacity (community-ambulating, home-ambulating, and not-ambulating) and gender. We also intent to compare the delay in bone age of the affected side compared to the unaffected side in patients with hemiparetic cerebral palsy.

CASUISTRY AND METHODS

Case series

We evaluated children with spastic CP, who were being followed at the Neuromuscular Diseases Clinic and underwent radiographs of the right and left wrists and hands, in anteroposterior incidence. The research was evaluated and approved by the Hospital's Ethics Research Committee (439/09). Radiographs and collection of patient data was authorized by a parent or guardian for each patient. Inclusion criteria were patients with spastic CP, skeletally immature, and therefore excluded children who completed the bone maturity, and presence of those with severe deformities that impair radiographic evaluation. The sample was represented by 450 patients without prior evaluation, of which 49 were excluded due to poor quality or absence of radiographic data in medical records. Of the 401 patients analyzed, 214 (53.3%) males and 187 (46.7%) females. Chronological ages ranged from 3 months to 20 years old (mean and median). Regarding the type of spastic lesion, patients were as follows: 149 were hemiparetic (37.2%), 128 diparetic (31.9%) and 124 quadriparetic (30.9%). Regarding the motor functional status, 182 were community-ambulating (45.4%), 52 home-ambulating (13%) and 167 non-ambulating (41.6%). (Table 1)

METHODS

The radiographs were evaluated by two independent observers, the bone age of the left and right wrist was determined according to the atlas Greulich and Pyle.¹⁰ The arithmetic mean of the measurements of the two observers was used for comparisons with chronological age.

The collected data were distributed in a spreadsheet: hospital records, initials, date of birth, gender, functional status (community-ambulating, home-ambulating, and not-ambulating), chronological age (in months ), bone age of the right and left wrist rated by observer 1, and the same for observer 2 , the arithmetic mean between observers 1 and 2 regarding bone age of the wrist and the left and right kind of spasticity (hemiparesis, diparesis, and tetraparesis).

Regarding the hemiparetic patients there were recorded separately the affected and not affected sides, since the side without spasticity would be the control group.

The status of ambulation was the criterion to assess the severity of spasticity, therefore the impairment in increasing order of severity would be: community-ambulating (1), home-ambulating (2) and non- ambulating (3). It was also determined the influence of gender on the delayed bone age.

To assess the qualitative variables, we calculated absolute and relative frequencies; for quantitative variables, we calculated summary measurements. A comparison of the differences between chronological and bone age was performed using the Student's t test or variance analysis, and the comparison between the bone ages of affected and unaffected sides in hemiparetic patients was performed using the Student's t test for paired data. Assessment of inter-observer matching was made through the intra-class correlation coefficient. The level of significance adopted was 5 % (p < 0,05). The software used was SPSS (Statistical Package for the Social Sciences) version 13.0 for Windows.

RESULTS

Assessment of inter-observer matching resulted in high correlation coefficients with values of 0.995 and 0.994 on the right and left sides, respectively. Given this result, it was possible to confirm the reproducibility of the method to obtain bone age in patients with cerebral palsy between different observers and correlate them with several factors. (Table 2)

When comparing chronological age with the average bone age between the right and left wrist, according to the gender, we observed a delay in males of 13.59 months and in females of 9.63 months, showing only a tendency to a greater difference in males, without statistical significance (p = 0.54). (Table 3)

Regarding the topographic distribution of the CP there was a significant delay (p <0.005) in tetraparetic (17.7 months), hemiparetic (10.1 months) and diparetic (7.9 months) patients. It was also evident a shorter delay in diparetic than in hemiparetic. (Table 4)

In the hemiparetic group, the mean bone age in the affected side was 96.88 months and in the unaffected side 101.13 months. The difference between both sides is statistically significant (p <0.005). (Table 5)

Regarding the functional status, the non-ambulating demonstrated a significant delay in bone age over the chronological age of 18.73 months (p <0.005). The delay in community-ambulating was 6.72 months and in the home-ambulating 6.93 months, both showing no statistically significant difference (p=1 in both). (Table 6)

DISCUSSION

Analyzing the results obtained, we observe that patients with spastic CP showed delayed bone age compared with chronological age. However, these data were based on the book from Greulich and Pyle,¹⁰ which could assume that our healthy population could also present this delay due to the socio-economic and cultural reasons. But the fact that we have studied patients with hemiplegia, in which the normal side was the control group, and the fact that we have also observed a delay in the affected side compared to the unaffected, not only corroborates this statement, but we can also correlate with the involvement of non-nutritional factors.^6,8,9,11,12 Regarding the severity of spasticity we ranked patients according to ambulating status , despite other methods are available, such as quantifying the degree of skills in the upper limb (QUEST -Quality of Upper Extremity Skills Test).^6,7 The GMFCS test, one of the most commonly used method in functional ranking of patients with spastic cerebral palsy, was not included in this paper because it is a retrospective study with data collection from the patient's charts. We are aware about the difficulty to to differentiate between home-ambulating patients and community-ambulating in some cases, but it is a fact for not-ambulating patients. Therefore, we observe a longer delay in bone age of non-ambulating in comparison to ambulating, without evident difference between homeand community-ambulating. Regarding the type of spastic CP we observed a significant delay in bone age between the hemiparetic and tetraparetic and a smaller delay in diparetic. Regarding the non-ambulating status we observe a higher occurrence among tetraparetic (95%) than in hemiparetic (21%) and diparetic (14%). Therefore, the delay in bone age may be related to the fact that the patient does not walk, thus influencing the final outcome of such a comparison. Even so, tetraparetic patients showed a longer development delay, and this may be related to nutritional and non-nutritional factors.^{6,7,9-11,13,14}

Erikcson et al.¹⁵ in a study with 38 patients with hemiparetic CP found no statistically significant difference between chronological age and bone age using the method of Greulich and Pyle¹⁰, unlike our results. However, the study had a small sample and only one observer.

In another study, Gilbert et al.¹⁶ observed no statistical difference between bone and chronological age in patients with tetraplegic paralysis. The authors used to the Fels method¹⁸ to determine bone age, considered by them complex and difficult to apply.

Will sometime during the growth bone age in patients spastic CP reaches the normal chronological age? Questions like this point out the need for a longitudinal study to further clarification. Although statistically not significant (p=0.54), males showed a delay compared to females, as described by Marcondes et al.¹⁴ and by Castro et al.,¹⁷ probably related to pubertal sexual development in CP affected children. In patients with cerebral palsy spastic hemiparesis it has been observed longer delay in the affected side compared to the unaffected.

The results are important, since indications of clinical and surgical treatment should take into account the real bone age, and provide interventions to reduce the backlog of patients with cerebral palsy compared with the general population.

For a more detailed study of the causes that potentially influence the rate of development of CP patients it would be necessary to develop an experimental model that controls the inherent defects and neurological impairment.

CONCLUSION

There is a delay in bone age compared with chronological age in patients with spastic CP, influenced by the topographic distribution of spasticity, functional level and gender. Tetraparetic patients had higher delayed bone age compared to hemiparetic and diparetic. It was observed a tendency to a greater delay in males compared to females.

Regarding the functional level, non-ambulating patients showed greater delay in bone age in relation to the chronological age, but no such difference was observed in community-ambulanting and home-ambulating patients. We can infer the influence of nutritional and non-nutritional factors on developmental delay in bone age in patients with spastic cerebral palsy.

REFERENCES

Article received in 09/21/2010, approved in 07/31/2011

All the authors declare that there is no potential conflict of interest referring to this article.

Work performed at Experimental Medicine and Clinical Research Unit (EMCRU) of Kocaeli University, Kocaeli-Turkey.

• 1. Bax MC. Terminology and classification of cerebral palsy. Dev Med Child Neurol. 1964;6:295-7.
• 2. Herring JA. Disorders of the brain. In: Tachdjian MO, Herring JA, editors. Tachdjian's pediatrics orthopedics. 4th ed. Philadelphia: Saunders; 2008. p.1275-404.
• 3. Samilson RL. Orthopaedic aspects of cerebral palsy. Philadelphia: J.B. Lippincott; 1975.
• 4. Hoffer MM, Feiwell E, Perry R, Perry J, Bonnett C. Functional ambulation in patients with myelomeningocele. J Bone Joint Surg Am. 1973;55(1):137-48.
• 5. 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. Dev Med Child Neurol. 1997;39(4):214-23.
• 6. Stevenson RD, Roberts CD, Vogtle L. The effects of non-nutritional factors on growth in cerebral palsy. Dev Med Child Neurol. 1995;37(2):124-30.
• 7. Roberts CD, Vogtle L, Stevenson RD. Effect of hemiplegia on skeletal maturation. J Pediatr Orthop. 1994;125(5):824-8.
• 8. Stevenson RD, Hayes RP, Cater LV, Blackman JA. Clinical correlates of linear growth in children with cerebral palsy. Dev Med Child Neurol. 1994;36(2):135-42.
• 9. Kong CK, Tse PW, Lee WY. Bone age and linear skeletal growth of children with cerebral palsy. Dev Med Child Neurol. 1999;41(11):758-65.
• 10. Greulich WW, Pyle SI. Radiographic atlas of skeletal development of the hand and wrist. 2nd ed. Standford: Stanford University Press; 1959.
• 11. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33(1):159-74.
• 12. Stallings VA, Charney EB, Davies JC, Cronk CE. Nutrition-related growth failure of children with quadriplegic cerebral palsy. Dev Med Child Neurol. 1993;35(2):126-38.
• 13. Tobis JS, Saturen P, Larios G, Posniak AO. Study of growth patterns in cerebral palsy. Arch Phys Med Rehabil. 1961;42:475-81.
• 14. Marcondes E, Valente MI, Fiore FF, Coelho Neto AS. Idade óssea em crianças com paralisia cerebral. Arq Neuropsiquiatr.1965;23(2):127-35.
• 15. Erickson T, Loder RT. Bone age in children with hemiplegic cerebral palsy. J Pediatr Orthop. 2003;23(5):669-71.
• 16. Gilbert SR, Gilbert AC, Henderson RC. Skeletal maturation in children with quadriplegic cerebral palsy. J Pediatr Orthop. 2004;24(3):292-7.
• 17. [50] Roche AF, Chumlea WmC, Thissen D. Assessing the Skeletal Maturity of the Hand-Wrist: FELS Method. Charles C. Thomas; Springfield: 1988.
• 18. Castro M, Nicolas J, Palestini MP, Patri A, Valenzuela C. Desarrollo sexual puberal en niños con parálisis cerebral. Pediatría (Santiago de Chile);1989;32(2):96-100.

Publication Dates

• Publication in this collection
  05 Nov 2013
• Date of issue
  2013

History

• Received
  21 Sept 2010
• Accepted
  31 July 2011