Abstract

INTRODUCTION

The term cerebral palsy (CP) is frequently used to designate a large number of clinical conditions which have in common a specific and non-progressive lesion in the immature brain.¹ It is related, among other conditions, to movement disorders, such as lack of selective muscle control and muscle imbalance. It is traditionally classified by the clinical type (motor dysfunction) and topography (anatomical region of the lesion). There are some types of motor dysfunction, such as spastic, the most common type, ataxic, hypotonic, dyskinetic (choreo-athetotic, or dystonic) and mixed. The anatomical distribution patterns are generally classified as hemiplegic, diplegic and quadriplegic. Although classifications by motor dysfunction and topography have been widely used, there is no mention about function in it.

The Gross Motor Function Classification System (GMFCS)²2. Palisano RJ, Hanna SE, Rosenbaum PL, Russell DJ, Walter SD, Wood EP, et al. Validation of a model of gross motor function for children with cerebral palsy. Phys Ther. 2000;80(10):974-85. is a simple, reliable, easily reproducible, and widely used classification based on gross motor function and consists of five distinct functional levels. The classification into levels is based on the patient's usual motor performance, the quality of movement at home and in community settings and the need for assistive technologies. Motor level I includes patients with the least severe motor impairments and motor level V includes patients with the most severe functional limitations. The use of GMFCS has added important information about function in children with CP, but a diversity of gait patterns can be present even in the same functional level. Because of it, many efforts have been made to develop classification or quantification systems for it to assist in clinical diagnosis, decision making and communication.³3. Dobson F, Morris ME, Baker R, Graham HK. Gait classification in children with cerebral palsy: a systematic review. Gait Posture. 2007;25(1):140-52.

One of these systems is the Gait Deviation Index (GDI),⁴4. Schwartz MH, Rozumalski A. The Gait Deviation Index: a new comprehensive index of gait pathology. Gait Posture. 2008;28(3):351-7. which combines information of kinematic data obtained by the three-dimensional motion assessment in the gait laboratory. It allows the characterization of gait in patients by quantifying the overall quality of gait movements using nine kinematic variables. GDI equal to or greater than 100 indicates absence of gait pathologies. Every 10 points below 100 means one standard deviation away from the normal gait pattern. GDI is quantitative and provide an overview of kinematics, but its use is restricted to gait laboratories.

Sutherland and Davids⁵5. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;(288):139-47. described four pathological gait patterns based on knee motion in the sagittal plane: jump, recurvatum, crouch and stiff knee. Rodda et al.⁶6. Rodda JM, Graham HK, Carson L, Galea MP, Wolfe R. Sagittal gait patterns in spastic diplegia. J Bone Joint Surg Br. 2004;86(2):251-8. classified the gait patterns in spastic diplegic CP into five groups, based on the kinematic analysis in the sagittal plane of the ankle, knee, hip and pelvis. These two classifications systems have similar characteristics, but the classification of Sutherland and Davids⁵5. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;(288):139-47. is simpler and easier to apply in a large group of patients.

The purpose of this study was to test the use of Sutherland and Davids classification⁵5. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;(288):139-47. in a large group of children with spastic diplegic CP, identifying the prevalence of the four patterns described (jump, recurvatum, crouch and stiff knee). The secondary objective was to characterize each pattern based on age, GMFCS, GDI and surgical history. According to the authors' knowledge, the present study is the first in achieving prevalence and characterization of gait patterns described by Sutherland and Davids⁵5. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;(288):139-47. in a large group of children with cerebral palsy.

PATIENTS AND METHODS

A retrospective cross-sectional study was conducted using the database of the gait laboratory of a tertiary hospital and rehabilitation center, which was approved by the local ethics committee. A search was done for all patients with spastic diplegic CP who underwent gait analysis between 1996 and 2012. Among the 2,928 exams previously selected, only the first examination of each patient was included in the study, for a total of 1,805 patients.

In order to collect kinematic data, reflective markers were strategically placed on specific anatomical landmarks on the participants, as described by Kadaba et al.⁷7. Kadaba MP, Ramakrishnan HK, Wootten ME. Measurement of lower extremity kinematics during level walking. J Orthop Res. 1990;8(3):383-92. The trajectory of the markers within the lab space was captured through an electronic optical system consisting of infrared cameras. Until August 2008, a 6-camera Vicon 370 system (60 Hz) was used for data capture, and from this date on, an 8-camera QUALISYS OQUS300 system (500 Hz) was used.

Patients were instructed to walk barefoot in a self-selected speed in an eight-meter walkway (26 feet). A minimum of 10 gait cycles for each assessed leg was collected for consistency evaluation. The data were processed using the software Vicon Clinical Manager (VCM, Oxford Metrics, Oxford, UK) according to the technique described by Davis et al.⁸8. Davis RB, Ôunpuu S, Tyburski DJ, Gage JR. A gait analysis data collection and reduction technique. Hum Mov Sci. 1991;10:575-87. Only consistent cases were considered and the analysis was performed from the average of the 10 collected cycles. For data analysis, patients were divided into groups based on the classification proposed by Sutherland and Davids⁵5. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;(288):139-47. (jump, crouch, recurvatum, and stiff knee). Patients allocated to the jump-knee group showed the first peak knee flexion above 30° followed by minimum flexion in single support from 10° to 20° in kinematics. Patients classified as crouch knee gait had minimum knee flexion greater than 30° in stance phase. Patients with recurvatum knee gait showed knee extension below 0° in stance phase. Individuals classified into the stiff knee gait group exhibited peak knee flexion in swing phase limited to a maximum of 45° or late peak knee flexion in more than 30% of the swing phase. Besides these groups, patients were classified into groups exhibiting asymmetrical gait pattern when the knees showed different patterns between right and left sides. Patients were classified as mixed pattern when more than one pattern described by Sutherland and Davids⁵5. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;(288):139-47. was observed in the same knee. Finally, the last group consisted of patients who do not fit into any of the foregoing patterns.

The variables age, GMFCS, GDI and previous surgeries (at gastrocnemius-soleus complex, hamstrings and rectus femoris) were analyzed for each individual. We included children with previous surgeries in the study in order to evaluate the potential relationship between the procedure and specific gait patterns. All data were analyzed and comparisons were performed by ANOVA, using the software SPSS V17, Minitab 16 and Office Excel 2010. For comparisons between groups, Tukey's multiple comparison test was applied as well, and the level of significance for all tests was settled on 0.05 (5%).

RESULTS

The analysis of 1,805 patients resulted in the following distribution among groups: crouch knee gait with 395 patients (21.88%); jump knee gait with 168 patients (9.30%); stiff knee gait with 32 patients (1.77%); recurvatum knee gait with 70 patients (3.87%); asymmetrical pattern with 881 patients (48.80%); mixed pattern with 31 patients (1.70%) and non-classified group with 228 patients (12.68%).

Regarding age, the groups with jump and recurvatum knee gait had the lowest means compared with the other groups, with mean ages of 9.0 and 9.4 years old, respectively. There was no significant difference between these two groups as well as among the other groups. (Table 1)

Patients of the crouch knee group had the lowest GDI values (43.58), while the non-classified group exhibited the highest values (64.12). (Table 2) The patients of jump knee (58.91), asymmetrical pattern (56.65), recurvatum knee (56.86) and stiff knee (56.64) groups were not significantly different. The patients of group with mixed pattern showed mean GDI (50.94) lower than those of non-classified and jump knee groups and higher than the crouch group. There was no significant difference among the asymmetric, recurvatum, stiff and jump knee groups.

There were more children classified within GMFCS level III in the mixed and crouch groups (70% and 57.8%, respectively), and level II in the remaining groups (Jump 50.3%, Non-Classified 46.6%, Asymmetrical 44.7%, Stiff 41.9% and Recurvatum 40%). (Table 3 A, B)

The groups with jump and recurvatum knee patterns underwent significantly less triceps surae lengthening procedures than the stiff, crouch, asymmetrical and mixed groups. (Table 4)

The jump knee group showed the lowest percentage of previous hamstrings surgical lengthening, with significantly lower value than the other groups, except for the recurvatum knee group. On the other hand, the stiff knee group exhibited the highest percentage of previous hamstrings surgery compared with the other groups, except for the mixed group. (Table 5)

The highest percentage of the rectus femoris transfer was observed in the crouch group, with value significantly higher than those of the asymmetrical, jump and non- classifiable groups. (Table 6)

DISCUSSION

In the present study the asymmetrical group was the most frequent (48.8%) and only 36.82% of patients were classified according to patterns described by Sutherland and Davids.⁵5. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;(288):139-47. The groups with jump and recurvatum knee gait had the lowest age compared with the other groups, with means of 9.0 and 9.4 years old, respectively. Patients of the crouch knee group had the lowest GDI values (43.58), while the non-classified group exhibited the highest values (64.12). There were more children classified within GMFCS level III in the mixed and crouch groups (70% and 57.8%, respectively). The groups with jump and recurvatum knee patterns underwent significantly less triceps surae lengthening procedures and the highest percentage of the rectus femoris transfer was observed in the crouch group. The jump knee group showed the lowest percentage of previous hamstrings surgical lengthening and the stiff knee group exhibited the highest.

Rodda et al.⁹9. Rodda J, Graham HK. Classification of gait patterns in spastic hemiplegia and spastic diplegia: a basis for a management algorithm. Eur J Neurol. 2001;8(Suppl 5):98-108. also found a substantial number of patients with asymmetrical impairments between sides and designed a classification system according to involved limbs, not by individual patients, in a longitudinal study on the natural progression of the disease. The present study has a cross-sectional design and it did not evaluate the natural history. The main purpose was to identify the prevalence of most frequent patterns in a large group of CP patients and the design applied is appropriate for this study.

The group of patients who did not fit in any of the primary classifications (12.68%) was apparently characterized by less severe impairments, exhibiting the highest GDI and prevalence of GMFCS II. The GDI combines information of kinematic data obtained by the three-dimensional motion assessment in the gait laboratory. It allows the characterization of gait in patients by quantifying the overall quality of gait movements using nine kinematic variables. GDI equal to or greater than 100 indicates absence of gait pathologies. Every 10 points below 100 means one standard deviation away from the normal gait pattern.⁴4. Schwartz MH, Rozumalski A. The Gait Deviation Index: a new comprehensive index of gait pathology. Gait Posture. 2008;28(3):351-7. Lin et al.¹⁰10. Lin CJ, Guo LY, Su FC, Chou YL, Cherng RJ. Common abnormal kinetic patterns of the knee in gait in spastic diplegia of cerebral palsy. Gait Posture. 2000;11(3):224-32. also found a group of patients showing a better gait pattern with absence of specific kinematics changes of the knee, which highlights the need for more detailed classifications for this group of patients as well.

The group of patients in which more than one pattern, of those described by Sutherland and Davids,⁵5. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;(288):139-47. was observed in the same knee is apparently characterized by relatively more severe impairments, with the second lowest GDI and prevalence of patients with GMFCS III. The stiff-knee gait pattern is the only one which refers to changes in the knee motion during the swing phase and may be present as part of another pathological knee pattern during the stance phase, therefore, it should not be regarded as a single and individual pattern.⁵5. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;(288):139-47.

The second largest group observed in this study is the crouch gait group, which is in agreement with results obtained by Wren et al.¹¹11. Wren TA, Rethlefsen S, Kay RM. Prevalence of specific gait abnormalities in children with cerebral palsy: influence of cerebral palsy subtype, age, and previous surgery. J Pediatr Orthop. 2005;25(1):79-83. in 2004. In that study, however, the highest prevalence was the stiff-knee gait pattern. It is the group of patients with the most severe impairment, which GDI was the lowest, with prevalence of GMFCS III patients. The highest incidence of previous rectus femoris transfer was observed in this group. Although previous studies have shown that the rectus femoris muscle does not actively participate in the knee extension during the stance phase of the normal gait,¹²12. Nene A, Byrne C, Hermens H. Is rectus femoris really a part of quadriceps? Assessment of rectus femoris function during gait in able-bodied adults. Gait Posture. 2004;20(1):1-13. ^{, 13}13. Arnold AS, Anderson FC, Pandy MG, Delp SL. Muscular contributions to hip and knee extension during the single limb stance phase of normal gait: a framework for investigating the causes of crouch gait. J Biomech. 2005;38(11):2181-9. other studies demonstrate increased knee flexion after surgery in the long term.¹⁴14. Saw A, Smith PA, Sirirungruangsarn Y, Chen S, Hassani S, Harris G, Kuo KN. Rectus femoris transfer for children with cerebral palsy: long-term outcome. J Pediatr Orthop. 2003;23(5):672-8.

15. Carney BT, Oeffinger D, Gove NK. Sagittal knee kinematics after rectus femoris transfer without hamstring lengthening. J Pediatr Orthop. 2006;26(2):265-7. ^{- 16}16. Rethlefsen SA, Kam G, Wren TA, Kay RM. Predictors of outcome of distal rectus femoris transfer surgery in ambulatory children with cerebral palsy. J Pediatr Orthop B. 2009;18(2):58-62.

The groups jump and recurvatum knee were formed by the youngest patients, which is in accordance to the description given by Sutherland and Davids.⁵5. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Relat Res. 1993;(288):139-47. These authors associate both the jump and the recurvatum knee to the triceps surae spasticity or contracture. They are also the patients with the lowest number of previous surgeries, as described by Wren et al.,¹¹11. Wren TA, Rethlefsen S, Kay RM. Prevalence of specific gait abnormalities in children with cerebral palsy: influence of cerebral palsy subtype, age, and previous surgery. J Pediatr Orthop. 2005;25(1):79-83. who reported the effectiveness of surgeries, in general, in reducing the likelihood of having ankle equinus.

The group of patients with exclusively stiff knee pattern during swing phase had the highest incidence of previous surgeries. Patients in the group of stiff gait pattern showed the highest rate of hamstring lengthening; however, none of them underwent rectus femoris transfer. The co-spasticity of the hamstrings and quadriceps in the swing phase is very common¹⁵15. Carney BT, Oeffinger D, Gove NK. Sagittal knee kinematics after rectus femoris transfer without hamstring lengthening. J Pediatr Orthop. 2006;26(2):265-7. and the masking of the rectus femoris muscle dysfunction by hamstring shortening was also described by Wren et al.¹¹11. Wren TA, Rethlefsen S, Kay RM. Prevalence of specific gait abnormalities in children with cerebral palsy: influence of cerebral palsy subtype, age, and previous surgery. J Pediatr Orthop. 2005;25(1):79-83. in 2004. The group with stiff knee gait pattern also had one of the highest rates of triceps surae lengthening (53.1%). Although many authors do not agree with the role of plantar flexors in propulsion generation (i.e., forward acceleration of the mass center),¹⁷17. Sutherland DH, Cooper L, Daniel D. The role of the ankle plantar flexors in normal walking. J Bone Joint Surg Am. 1980;62(3):354-63. there are new studies describing that elastic energy is stored in the tendon along the plantar flexors when they are stretched to the maximum at the end of the single support. This energy causes a rapid plantar flexion of the ankle in pre-swing, helps pushing the tibia forward and thus contributes to approximately 40° of knee flexion required at this stage of the cycle.¹⁸18. Perry J, Burnfield J. Gait analysis: normal and pathological function. 2nd ed. Thorofare: Slack Inc.; 2010. A possible weakness caused by plantar flexor lengthening can then interfere with this phenomenon, currently known as the fourth rocker mechanism, and lead to delay and limitation of peak knee flexion in the swing phase.

There was no relationship between the hyperextension of the knee and prior stretching of the hamstring. Based on this, we believe that the hyperextension of the knee in the studied sample is rather primary than iatrogenic.

The present study has some limitations. As described, it is a cross-sectional study, designed in order to determine the prevalence of most frequent gait patterns in a large group of cerebral palsy patients and characterize them. The study does not provide information about natural history and the inclusion of patients with previous surgeries can be a confounding factor, however the medical history of each patient, including previous surgeries, is an important issue for the characterization of groups. As observed in the present data, specific gait patterns exhibited relation with previous surgery and these findings should be investigated in the future using a different study design. On the other hand, the results have significant clinical implications. The determination of most frequent gait patterns prevalence in a population is important for planning treatment approaches and resources. In addition to this, when gait analysis was applied, a substantial number of asymmetrical patients were identified, even in a group of diplegic spastic CP. This information should be considered during a decision making process in clinical setting, because part of treatment indications can be asymmetrical, even in children with diplegic spastic CP.

CONCLUSION

In conclusion, only 36.82% of the studied patients were classified according to the classic patterns. The asymmetrical cases were more frequent within a group of diplegic patients. Individuals with crouch gait pattern were characterized by the lowest GDI, the highest prevalence of GMFCS III and previous rectus femoris transfer, while patients with stiff knee exhibited a higher percentage of previous hamstring lengthening in comparison with other groups.

REFERENCES

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