Cortical bone deficit and fat infiltration of bone marrow and skeletal muscle in ambulatory children with mild spastic cerebral palsy

Abstract

Introduction: Nonambulatory children with severe cerebral palsy (CP) have underdeveloped bone architecture, low bone strength and a high degree of fat infiltration in the lower extremity musculature. The present study aims to determine if such a profile exists in ambulatory children with mild CP and if excess fat infiltration extends into the bone marrow.

Materials and methods: Ambulatory children with mild spastic CP and typically developing children (4 to 11years; 12/group) were compared. Magnetic resonance imaging was used to estimate cortical bone, bone marrow and total bone volume and width, bone strength [i.e., section modulus (Z) and polar moment of inertia (J)], and bone marrow fat concentration in the midtibia, and muscle volume, intermuscular, subfascial, and subcutaneous adipose tissue (AT) volume and intramuscular fat concentration in the midleg. Accelerometer-based activity monitors worn on the ankle were used to assess physical activity.

Results: There were no group differences in age, height, body mass, body mass percentile, BMI, BMI percentile or tibia length, but children with CP had lower height percentile (19th vs. 50th percentile) and total physical activity counts (44%) than controls (both p<0.05). Children with CP also had lower cortical bone volume (30%), cortical bone width in the posterior (16%) and medial (32%) portions of the shaft, total bone width in the medial-lateral direction (15%), Z in the medial-lateral direction (34%), J (39%) and muscle volume (39%), and higher bone marrow fat concentration (82.1±1.8% vs. 80.5±1.9%), subfascial AT volume (3.3 fold) and intramuscular fat concentration (25.0±8.0% vs. 16.1±3.3%) than controls (all p<0.05). When tibia length was statistically controlled, all group differences in bone architecture, bone strength, muscle volume and fat infiltration estimates, except posterior cortical bone width, were still present (all p<0.05). Furthermore, a higher intermuscular AT volume in children with CP compared to controls emerged (p<0.05).

Conclusions: Ambulatory children with mild spastic CP exhibit an underdeveloped bone architecture and low bone strength in the midtibia and a greater infiltration of fat in the bone marrow and surrounding musculature compared to typically developing children. Whether the deficit in the musculoskeletal system of children with CP is associated with higher chronic disease risk and whether the deficit can be mitigated requires further investigation.

Keywords: Bone strength; Bone structure; Cerebral palsy; Fat depots; Unloading.

Figure 1

A general description of the image processing procedure used to quantify bone architecture and strength of the midtibia and the fat infiltration of the bone marrow and surrounding musculature. Raw T1-weighted magnetic resonance images (A) were segmented (B) into tibia cortical bone (large black ring; fibula is the small black ring) and bone marrow (white region surrounded by the cortical bone), muscle (gray region surrounding the bone) and adipose tissue (AT; white ring surrounding the muscles and bones and the white voxels interspersed among the musculature). The bone, muscle and AT volumes, bone widths (cortical bone in the anterior, posterior, medial and lateral portions and the bone marrow and total bone in the anterior-posterior and medial-lateral directions) and estimates of bone strength (section modulus in the anterior-posterior and medial-lateral directions and polar moment of inertia) were calculated. Voxels identified as bone marrow and muscle were applied to fat (C) and water (D) images to determine bone marrow and intramuscular fat concentration [25].

Figure 2

Estimates of bone strength [section modulus in the anterior-posterior (Z_ap) and medial-lateral (Z_ml) directions and polar moment of inertia (J)] in the midtibia of children with cerebral palsy (CP) and typically developing children (Con). *Group difference, p < 0.05. **Group difference, p = 0.057.

Figure 3

Bone marrow fat concentration (%) in the midtibia of children with cerebral palsy (CP) and typically developing children (Con). *Group difference, p < 0.05.

Figure 4

Intramuscular fat concentration (%) in the midtibia of children with cerebral palsy (CP) and typically developing children (Con). *Group difference, p < 0.05.

Figure 5

Raw T1-weighted magnetic resonance images from the midtibia demonstrate the marked deficit in bone architecture and muscle volume and the high infiltration of fat within and around the musculature in an ambulatory boy with mild CP (A) compared to a typically developing boy with the same tibia length (B). In the image of the child with CP (A), the small black arrow highlights the thin cortical shell and the large arrow highlights the fat infiltration of muscle.