Next Article in Journal
Frequency Response Analysis: An Enabling Technology to Detect Internal Faults within Critical Electric Assets
Previous Article in Journal
Multi-Output Regression with Generative Adversarial Networks (MOR-GANs)
Previous Article in Special Issue
How the Direction of Screws Affects the Primary Stability of a Posterior Malleolus Osteosynthesis under Torsional Loading: A Biomechanical Study
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Role of Knee Flexors Hypertonia in the Decision-Making of Hamstring Lengthening Surgery for Individuals with Cerebral Palsy

by
Faustyna Manikowska
1,*,
Sabina Brazevič
1,
Marek Jóźwiak
1 and
Maria K. Lebiedowska
2
1
Department of Pediatric Orthopedics and Traumatology, Poznań University of Medical Sciences, 61-701 Poznań, Poland
2
Independent Researcher, Edmonton, AB T5R 2R2, Canada
*
Author to whom correspondence should be addressed.
Appl. Sci. 2022, 12(18), 9210; https://doi.org/10.3390/app12189210
Submission received: 5 August 2022 / Revised: 9 September 2022 / Accepted: 10 September 2022 / Published: 14 September 2022

Abstract

:
Popliteal angle (PA) and the knee position at the end of the swing phase during walking (Kts) are considered criteria for treatment selection and outcome prediction of hamstring lengthening surgery in individuals with cerebral palsy (CP). However, the relationships among Kts, PA, and hypertonia are not clear. This study aimed to determine whether hamstrings hypertonia affects the values of PA and Kts, and how it may affect the hamstring lengthening decision for CP. One hundred and twenty-six subjects with CP (male = 72, female = 54; age = 11.1 ± 3.9 years) underwent gait analysis and examination of hamstrings hypertonia (Tardieu scale) and length (PA). We found that Kts increased with PA (Kts = 5.00 + 0.31 × PA (r = 0.39; p < 0.001)). Every 10° change of PA leads to 3° improvement of knee position in walking. Kts were larger (p < 0.001) in the limbs with (20.40 ± 11.27°) than without (15.60 ± 9.99°) knee flexors hypertonia (Tardieu slow); and were larger (p < 0.001) in the limbs with (20.39 ± 11.01°) than without (14.85 ± 9.89°) knee flexors hypertonia (Tardieu fast). PAs were larger (p < 0.05) in the limbs with (42.81 ± 12.66°) than without (38.96 ± 14.38°) hypertonia (Tardieu fast). Kts = 13.93° and PA = 30° were cutoff values of the presence of hypertonia with sensitivities of 75.0% and 89.1%, respectively. Kts increased with the PA in ambulatory CP. It is estimated that pathological increase of Kts occurs at PA ≥ 40°. The hypertonia of knee flexors affected Kts and PA. The presence of knee flexors hypertonia should be considered in the decision-making of hamstring lengthening for individuals with CP if Kts ≥ 13.93° and PA ≥ 30°.

1. Introduction

Cerebral palsy (CP) is a group of neuromuscular disorders caused by early injury of the brain region involving movement pathways control. Neuromuscular deficits lead to functional limitations including abnormal gait patterns. Functional limitations are the consequences of complex impairments typical for upper motoneuron damage including weakness, lack of selective muscle control, and hypertonia due to spasticity and/or dystonia and/or muscle shortening.
The data from clinical tests and instrumental methods are used in daily clinical practice to determine an optimal treatment strategy. The popliteal angle (PA) test is commonly considered a passive assessment of the biomechanical properties of the knee flexors, in particular its length. During the standard PA procedure, the examiner extends the knee joint at a slow velocity while the examinee lies supine with the hip 90° flexed. The value of the PA may be related to increased resistance at the knee joint (Figure 1). The resistance may be increased due to biomechanical (muscle shortness) or neural factors (predominantly spastic hypertonia) as a result of velocity- or muscle-length-dependent stretch reflexes in patients with CP [1,2,3]. The most common tests for hypertonia include the modify Ashworth scale (MAS) and the Tardieu scale (TAS), where TAS better complies with the concept of spasticity evoked by either slow or fast stretch [4].
The instrumented three-dimensional gait analysis can quantify gait abnormality in individuals with neuromuscular deficits. Limited knee flexion range of motion (ROM) during gait is commonly observed in individuals with CP. The value of knee flexion at the end of the swing phase during walking (Kts) is one of the criteria for treatment selection (Figure 2). Both muscle shortness and spastic hypertonia may affect the knee ROM during walking. The exaggerated stretch reflexes in response to muscle stretch could affect gait [5,6,7,8,9]. As a consequence, it is difficult to differentiate whether limitations in dynamic knee ROM during walking originate from hypertonia or shortness of knee flexors.
The role of PA test as a criterion for hamstring lengthening surgery and as a predictor of knee flexion during walking is debatable because the conditions of testing on an examination bench are radically different than during walking [10]. Moreover, increasingly researchers emphasize the influence of hypertonia on PA test. The activation of ipsilateral and contralateral muscles of the legs has been reported [1,11,12]. The hamstring lengthening surgery is not always effective and the improvement of knee ROM during walking is not consistent across individuals [13,14,15]. Thus, muscle shortness may be only one of the contributing factors to gait pathology. Emerging data recognize improper links between neurological injury, neuromuscular deficits, and gait abnormalities in patients with CP. It seems that data obtained with gait analysis and clinical tests are not direct and obvious [16,17,18].
PA is a result of clinical evaluation performed on the examination table. However, the Kts is a knee position during walking which is a functional performance. Both values might be affected by hamstrings shortness and/or spastic hypertonia. It is unclear whether there exists an association between both of them. There is also no agreement on if different treatment procedures should be beneficial whether hypertonia is present or absent, especially since hypertonia may lead to, or coexist with, contractures. A better understanding of these relationships can lead to more effective treatment strategies.
The aims of the present study were:
  • To establish the association between PA and Kts in children with CP;
  • To determine whether hamstrings hypertonia affects the values of PA and Kts;
  • To determine the probabilities of inclusion for hamstring lengthening surgery limbs of patients with or without hypertonia based on the values of PA and Kts.
To achieve the above aims we analyzed the results of clinical tests: PA, muscle hypertonia (evaluated by TAS at both slow (i.e., Tardieu V1) and fast (i.e., Tardieu V3) velocities), and knee angular position at the end of swing (evaluated by instrumented gait analysis).

2. Materials and Methods

The appropriate Institutional Review Board approved the study (Approval No: 244/20 (11 March 2020), and written consent for using the examination data was acquired from all participants. For participants under the age of 18, consent was obtained from a parent or legal guardian.

2.1. Participants

In total, data from 126 individuals (male, n = 72; female, n = 54; age = 11.1 ± 3.9 years; 213 limbs) with spastic CP were retrospectively analyzed. All data were extracted from the database of the local gait analysis laboratory. Inclusion criteria were: (1) diagnosed as spastic CP; (2) no missing data in either clinical examinations or gait analysis. The exclusion criterion was any surgery or botulinum toxin within 6 months before the assessment.

2.2. Protocol

The selected gait parameters of patients were obtained through an eight-camera instrumented three-dimensional gait analysis system (Vicon, Vicon Motion Systems Ltd., Oxford, UK) sampling at 120 Hz. Fifteen reflective markers were attached to each participant based on the standard Plug-in-Gait model [19]. Data were collected only from the patients who were able to walk barefoot along the 10-m long examining walkway at least 3 times with or without the use of an assistive device. The Kts was measured for each gait cycle and the average values across the gait cycles were used in the analysis.
Selected clinical parameters were obtained through clinical evaluation of hamstrings muscle spasticity and measure of unilateral PA under standard positions [20,21]. Clinical examination was performed by experienced physical therapists with practice in the assessment of children with CP:
  • Unilateral popliteal angle test (PA) was performed on the examination table with the participant in a supine position; the opposite leg relaxed on the table with both hip and knee extended at the neutral position; the hip of the tested leg was flexed 90° and the examiner extended the knee. The angle was measured by a manual goniometer.
  • Hamstrings muscle spasticity (HYP) was graded by TAS from 0 to 5 (where 0 means no resistance throughout the passive movement; 1 = slight resistance throughout passive movement without a catch; 2 = clear catch at a precise angle; 3 = fatigable clonus < 10 s; 4 = non-fatigable clonus > 10 s; 5 = joint immovable) in two velocities: slow (vs) and as fast as possible (vf). The spastic hypertonia was categorized into two groups depending on the presence (YES; i.e., TAS = 1–5) or absence (NO; i.e., TAS = 0) of impairment.

2.3. Outcome Measures

Primary outcome measures for the study were data from clinical tests: PA, TAS at slow velocity (HYPvs), TAS at fast velocity (HYPvf), and knee angular position at the end of swing phase (Kts). Impairments of hypertonia (HYP) were categorized into two categories depending on the presence (YES) or the absence (NO) of it.
Secondary outcome measures were the cutoff values, i.e., the angular values of PA and Kts which separate the presence and absence of hypertonia (as evaluated with TAS), and angular values of PA which separate between presence and absence of lack of knee extension—Kts > 10° (taking into consideration the customarily accepted [22,23] 5° error of knee position measurement).

2.4. Data Analysis

Both PA and Kts were not normally distributed as confirmed with Kolmogorov–Smirnoff test and Spearman’s correlation and the linear regression equations were calculated to determine the association between them. To determine whether hamstrings muscle hypertonia affects the values of PA and Kts, Kruskal–Wallis ANOVA by ranks analysis was applied. To determine the probabilities of inclusion for hamstring lengthening surgery for patients with hamstrings shortening with or without hypertonia, we performed the sensitivity/specificity analysis of detection of hypertonia of hamstring muscles based on the spectrum of PA angle values (5.0–80.0°) and Kts values (0.6–52.6°).
The cutoff value for optimum sensitivity and specificity (to detect or not to detect hypertonia) of PA and Kts were calculated using receiver operating characteristic (ROC) analysis [24,25]. The strength of the impact was evaluated with the area under the sensitivity/specificity curve (AUC). The strength of the impact was evaluated with the area under the AUC where 1.0 means the strongest and 0.5 means no impact with a statistical significance of the p-value. Z-statistics were used to determine the statistical significance of the difference between the AUC and 0.5. The AUC scores ranged from 0.5 to 1.0: An AUC closer to 1.0 implied a stronger contribution of hypertonia on the PA/Kts value. The closer the AUC was to 0.5, the lower its contribution was. For the sake of the analysis, we defined the presence or absence of knee flexors hypertonia, which was based on the HYPvs and HYPvf.
Statistical analysis was performed with Statistica13™, StatSoft™ Ltd., and Stata Cytel with a level of significance at 0.05.

3. Results

3.1. Association between PA and Kts

We found that the knee flexion at the end of swing of walking (Kts) increased with the popliteal angle (PA) according to the equation:
K ts = 5.00 + 0.31 × PA
r = 0.39; p < 0.001 in the limbs of ambulatory patients with CP (Figure 3).
The results of receiver-operating characteristic (ROC) analysis (p = 0.05, AUC = 0.634) indicate that the cutoff value of PA to detect 10° and more of knee flexion in Kts is 40° (sensitivity = 69.7%, specificity = 56.3%). For PA ≥ 40° the probability of the presence of pathological knee flexion in Kts increases.

3.2. Effect of HYP on PA and Kts in Children with CP

Our data indicate that the presence or absence of clinically recognized hamstrings hypertonia affected almost all variables. Kts was affected (Kruskal–Wallis test: H(1,N = 213) = 12.56, p = 0.0004)) by the presence of hypertonia (as recognized with HYPvs) (Table 1).
Kts and PA were affected by the presence of hypertonia (as recognized with HYPvf) as examined with Kruskal–Wallis test: H(1,N = 213) = 16.26694, p = 0.0001 and H(1,N = 213) = 3.57, p = 0.05, respectively (Table 2).
The PA and Kts were larger in the limbs with clinically detected knee flexors hypertonia, but the differences were not statistically significant for PA when hypertonia had been identified using TAS at slow velocities (HYPvs). Kts were larger (p < 0.001) in the limbs with (20.4 ± 11.27°) than without (15.60 ± 9.99°) knee flexors hypertonia (HYPvs). At fast velocity (HYPvf), PAs were larger (p ≤ 0.05) in the limbs with (42.81 ± 12.66°) than without (38.96 ± 14.38°) hypertonia and Kts were larger (p < 0.001) in the limbs of patients with (20.39 ± 11.01°) than without (14.85 ± 9.89°) knee flexors hypertonia.

3.3. Probabilities of Inclusion for Hamstring Lengthening Surgery Patients with or without Hypertonia Based on the Values of PA and Kts

The analysis of sensitivity/specificity of Kts (Figure 4) to detect the presence of knee flexors hypertonia using ROC analysis (AUC = 0.66, p < 0.0001) (Table 3) indicates that 13.93° is the Kts cutoff value (sensitivity = 75%, specificity = 51.5%) to detect the absence of knee flexors hypertonia. The probability of absence of hypertonia (as detected with TAS at fast velocities HYPvf) decreases for Kts larger than 13.93°.
The analysis of sensitivity/specificity of PA (Figure 5) to detect the presence of knee flexors hypertonia using ROC analysis (AUC = 0.587, p = 0.022) (Table 3) indicates that 30° is the PA cutoff value (sensitivity = 89.07%, specificity = 25.44%) to detect the absence of knee flexors hypertonia. The probability of absence of hypertonia (as detected with TAS at fast velocities [HYPvf]) decreases for PA larger than 30°.
ROC analysis suggested that Kts ≥ 13.93° (sensitivity = 75.0%) and PA ≥ 30° (sensitivity = 89.1%) were affected by the presence of hypertonia.

4. Discussion

The first aim of the present study was to establish the association between popliteal angle (PA) and knee angle at the end of the swing phase in walking (Kts) in children with CP. We found a weak correlation between clinically obtained values of PA and Kts that suggests an association between them.
The differences between the conditions in which the clinical and instrumental data had been collected could be responsible for 15% of the variance of Kts due to PA. Taking into consideration that an increase in PA is related to an increase in Kts according to the equation Kts = 5.00 + 0.31 × PA (r = 0.39; p < 0.001) it can be estimated that a decrease in PA by 10° can lead to 3° improvement of knee position in walking. The value of the estimation can be tested using the data from pre- and post-surgery if available.
We found that the presence or absence of hamstrings hypertonia (clinically detected with TAS at slow and fast velocities) affected the majority of variables (Table 1 and Table 2). This suggests the contribution of hamstrings hypertonia to the increased values of PA and to an increased knee flexion at the end of swing (Aim 2). The values of PA and knee position at the end of swing were larger (from 11% to 39% when means were considered) in limbs with, rather than without, hypertonia. It had been previously acknowledged that the lack of knee extension at the end of swing may be related not only to hamstrings muscle shortness [26,27], but also to hamstrings muscle hypertonia and/or selective motor control impairment in a patient with CP [27,28,29,30,31]. Modelling data also suggest that other factors beyond hamstrings muscle shortness seem to affect knee position at the end of swing [32,33].
The associations between hamstrings spasticity, PA, and knee position at the end of swing remain debatable [34,35,36,37]. Both the presence [34,35,36] and absence [4,37] of such relationships have been previously reported. Muscle activation, also triggered by stretch reflexes leading to an increased resistance (hypertonia), is commonly reported in patients with CP [38].
It has been reported that PAs were larger when hamstrings were activated than when they were silent in the limbs of patients with CP [1,11,12,39].
Our data provide another argument to support the impact of hamstrings muscle spastic hypertonia on the increased PA values and an increased knee flexion at the end of swing phase of walking. The strength of the impact of each of the factors requires further studies to better customize the treatment to individual patients’ needs.
The application of ROC analysis allows the determination of the probabilities of inclusion for hamstring lengthening surgery for patients with or without hypertonia based on the cutoff values of PA and Kts. The results of ROC analysis not only conforms with another method that had been used in a previous aims to show that both Kts and PA can be used to differentiate patients’ limbs with the presence or absence of clinically tested hypertonia (Table 3), but also allows us to establish the cutoff values for such differentiation.
We found that Kts = 13.93° (AUC = 0.66, p < 0.0001) generates the cutoff value (sensitivity = 75%, specificity = 51.5%) to detect the absence of knee flexors hypertonia. For Kts ≥ 13.93° the probability of absence of hypertonia decreases rapidly (as detected with TAS at fast velocities) (Figure 4). The value of PA = 30° (AUC = 0.587, p = 0.022) generates the cutoff value (sensitivity = 89.07%, specificity = 25.44%) to detect the absence of knee flexors hypertonia. The probability of absence of hypertonia decreases for PA ≥ 30° (Figure 5). In addition, we found that the pathologically decreased knee extension at the end of swing Kts ≥ 10° [22,23] can be predicted with 69.7% of sensitivity and 56.3% of specificity when PA = 40° with rapidly increasing sensitivity for PA > 40°.
To our knowledge, our study provides original, analytically obtained cutoff values of PA and Kts during gait to detect the presence of knee flexors hypertonia based on two clinical tests: TAS at slow and TAS at fast velocities (HYPvs, HYPvf, respectively) (Table 3). The value of such analysis is supported by an effort to establish the criteria for knee flexors lengthening surgery based on the values of clinically tested PA and Kts, obtained during gait analysis, especially since it has been reported that they are affected as results of surgeries [5,11,12,15,40]. However, the improvement of knee position at the end of swing after hamstring lengthening was not always successful despite the fact of a decreasing value of PA [5,11,12,14,15,31,40].
It has been recently suggested that indications for hamstring lengthening surgery should focus on instrumented gait analysis data supplemented only by the results of clinical tests in ambulatory children with CP [41]. It has been advocated that the lack of extension especially Kts > 30° at the end of swing/initial stance should be used as a main criterion for the hamstring lengthening surgery. Our data do not question this criterion; however, we would like to emphasize that in 98% of ambulatory individuals with CP, Kts ≥ 30° indicates the coexistence of hypertonia (Figure 4). It seems that the interaction between muscle shortness and hypertonia should be considered before hamstring lengthening surgery [37] because the presence of hypertonia might influence the selection of appropriate treatment [42].
Theoretically, a hamstring lengthening surgery in the presence of muscle shortening and the absence of hypertonia should increase the knee extension range of the motion and result in both decrease in PA and knee flexion at the end of swing. Moreover, as a result of hamstring lengthening surgery the length of the muscle at certain positions is shorter, the knee flexors moment of force is smaller [43,44] and the stretch reflex activation also decreases with decreased muscle length as was found in human spasticity by Burke et al. in 1971. Thus, in both cases, the so-called muscle lengthening surgery could be beneficial to the normalization of the value of PA and functional improvement. Another important aspect of the interaction between contractures and hypertonia which requires further investigation is the potential effect of the type of hypertonia (velocity or position dependent), especially when a positive functional outcome of treatment, e.g., botulinum toxin injection, has been reported in the velocity- but not in the position-dependent hypertonia [10]. Future studies should reveal if different types of hamstring lengthening surgery (tendon vs. muscle) increase the muscle–tendon unit length, through a decrease (tendon) or increase (muscle) of muscle length that differently affect position- vs. velocity- dependent hypertonia.
In everyday clinical practice, not only the procedures but also arbitrary selection based on the experience and knowledge of individual orthopedic surgeons should also be accepted. Based on our data (Figure 3 and Figure 4), the probabilities of inclusion of patients with hypertonia based on the other arbitrary selected values of PA and Kts can be estimated for the first time.

Limitations

The present study focused on hypertonia only. Other factors and impairments may also contribute to gait abnormalities in patients with CP [45]. Impacts from other impairments should be addressed in future studies. Moreover, in this study, we considered all participants with CP as one group. Dividing them into different groups based on their Gross Motor Function Classification System (GMFCS) levels or severity of symptoms could complement our findings [37]. In addition, we defined the presence or absence of hypertonia based on the results of clinical TAS at slow and fast velocities. An instrumental evaluation of hypertonia should provide more precise and quantitative measures which should be used in future studies. Lastly, we did not investigate structural properties related to muscle shortness.

5. Conclusions

Kts increased with the PA in ambulatory individuals with CP. It is estimated that pathological increase of Kts occurs at PA ≥ 40°. The hypertonia of knee flexors affected Kts and PA. The presence of knee flexors hypertonia should be considered if Kts ≥ 13.93° and PA ≥ 30°, i.e., the cutoff values of the presence of hypertonia.

Author Contributions

Conceptualization, F.M. and M.K.L.; methodology, F.M. and M.K.L.; software, S.B.; validation, F.M., S.B., M.J. and M.K.L.; formal analysis, F.M., S.B. and M.K.L.; investigation, F.M. and S.B.; resources, M.J.; data curation, F.M., S.B., M.J. and M.K.L.; writing—original draft preparation, F.M. and M.K.L.; writing—review and editing, F.M., S.B., M.J. and M.K.L.; supervision, M.J. and M.K.L.; project administration, F.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Research Ethics Committees of Poznań University of Medical Sciences, Poland (approval #244/20 11 March 2020).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study. Written informed consent has been obtained from the patients to publish this paper.

Data Availability Statement

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Acknowledgments

The authors wish to thank Brian Po-Jung Chen for his perceptive editing of the paper.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Rha, D.-W.; Cahill-Rowley, K.; Young, J.; Torburn, L.; Stephenson, K.; Rose, J. Biomechanical and Clinical Correlates of Stance-Phase Knee Flexion in Persons With Spastic Cerebral Palsy. PM R 2016, 8, 11–18. [Google Scholar] [CrossRef]
  2. Louis, M.L.; Viehweger, E.; Launay, F.; Loundou, A.D. Peut-on Se Fier à L’angle Poplité Chez L’enfant Paralysé Cérébral Marchant? Rev. Chir. 2008, 94, 443–448. [Google Scholar]
  3. Cooney, K.M.; Sanders, J.O.; Concha, M.C.; Buczek, F.L. Novel Biomechanics Demonstrate Gait Dysfunction due to Hamstring Tightness. Clin. Biomech. 2006, 21, 59–66. [Google Scholar] [CrossRef]
  4. McMulkin, M.L.; Gulliford, J.J.; Williamson, R.V.; Ferguson, R.L. Correlation of Static to Dynamic Measures of Lower Extremity Range of Motion in Cerebral Palsy and Control Populations. J. Pediatr. Orthop. 2000, 20, 366–369. [Google Scholar]
  5. Bar-On, L.; Aertbeliën, E.; Molenaers, G.; Desloovere, K. Muscle Activation Patterns When Passively Stretching Spastic Lower Limb Muscles of Children with Cerebral Palsy. PLoS ONE 2014, 9, e91759. [Google Scholar]
  6. Lebiedowska, M.K.; Fisk, J.R. Knee Resistance during Passive Stretch in Patients with Hypertonia. J. Neurosci. Methods 2009, 179, 323–330. [Google Scholar] [CrossRef]
  7. van den Noort, J.C.; Scholtes, V.A.; Becher, J.G.; Harlaar, J. Evaluation of the Catch in Spasticity Assessment in Children with Cerebral Palsy. Arch. Phys. Med. Rehabil. 2010, 91, 615–623. [Google Scholar] [CrossRef]
  8. van Doornik, J.; Kukke, S.; Sanger, T.D. Hypertonia in Childhood Secondary Dystonia due to Cerebral Palsy Is Associated with Reflex Muscle Activation. Mov. Disord. 2009, 24, 965–971. [Google Scholar] [CrossRef]
  9. Scholtes, V.A.B.; Becher, J.G.; Beelen, A.; Lankhorst, G.J. Clinical Assessment of Spasticity in Children with Cerebral Palsy: A Critical Review of Available Instruments. Dev. Med. Child Neurol. 2006, 48, 64–73. [Google Scholar] [CrossRef]
  10. Bar-On, L.; Aertbeliën, E.; Van Campenhout, A.; Molenaers, G.; Desloovere, K. Treatment Response to Botulinum NeuroToxin-A in Children with Cerebral Palsy Categorized by the Type of Stretch Reflex Muscle Activation. Front. Neurol. 2020, 11, 378. [Google Scholar] [CrossRef]
  11. Manikowska, F.; Chen, B.P.-J.; Jóźwiak, M.; Lebiedowska, M.K. The Popliteal Angle Tests in Patients with Cerebral Palsy. J. Pediatr. Orthop. B 2019, 28, 332–336. [Google Scholar] [CrossRef]
  12. Sanger, T.D.; Chen, D.; Delgado, M.R.; Gaebler-Spira, D.; Hallett, M.; Mink, J.W. Taskforce on Childhood Motor Disorders Definition and Classification of Negative Motor Signs in Childhood. Pediatrics 2006, 118, 2159–2167. [Google Scholar] [CrossRef]
  13. Campbell, R.; Tipping, N.; Carty, C.; Walsh, J.; Johnson, L. Orthopaedic Management of Knee Joint Impairment in Cerebral Palsy: A Systematic Review and Meta-Analysis. Gait Posture 2020, 80, 347–360. [Google Scholar] [CrossRef]
  14. Osborne, M.; Mueske, N.M.; Rethlefsen, S.A.; Kay, R.M.; Wren, T.A.L. Pre-Operative Hamstring Length and Velocity Do Not Explain the Reduced Effectiveness of Repeat Hamstring Lengthening in Children with Cerebral Palsy and Crouch Gait. Gait Posture 2019, 68, 323–328. [Google Scholar] [CrossRef]
  15. Salami, F.; Brosa, J.; Van Drongelen, S.; Klotz, M.C.M.; Dreher, T.; Wolf, S.I.; Thielen, M. Long-Term Muscle Changes after Hamstring Lengthening in Children with Bilateral Cerebral Palsy. Dev. Med. Child Neurol. 2019, 61, 791–797. [Google Scholar] [CrossRef]
  16. Desloovere, K.; Molenaers, G.; Feys, H.; Huenaerts, C.; Callewaert, B.; Van de Walle, P. Do Dynamic and Static Clinical Measurements Correlate with Gait Analysis Parameters in Children with Cerebral Palsy? Gait Posture 2006, 24, 302–313. [Google Scholar] [CrossRef]
  17. Domagalska, M.; Szopa, A.; Syczewska, M.; Pietraszek, S.; Kidoń, Z.; Onik, G. The Relationship between Clinical Measurements and Gait Analysis Data in Children with Cerebral Palsy. Gait Posture 2013, 38, 1038–1043. [Google Scholar] [CrossRef]
  18. Zhou, J.; Butler, E.E.; Rose, J. Neurologic Correlates of Gait Abnormalities in Cerebral Palsy: Implications for Treatment. Front. Hum. Neurosci. 2017, 11, 103. [Google Scholar] [CrossRef]
  19. Davis, R.B.; Ounpuu, S.; Tyburski, D.; Gage, J.R. A Gait Analysis Data-Collection and Reduction Technique. Hum. Mov. Sci. 1991, 10, 575–587. [Google Scholar]
  20. Boyd, R.N.; Graham, H.K. Objective Measurement of Clinical Findings in the Use of Botulinum Toxin Type A for the Management of Children with Cerebral Palsy. Eur. J. Neurol. 2007, 6, s23–s35. [Google Scholar]
  21. Magee, L.A.; Pels, A.; Helewa, M.; Rey, E.; von Dadelszen, P. SOGC Hypertension Guideline Committee Diagnosis, Evaluation, and Management of the Hypertensive Disorders of Pregnancy: Executive Summary. J. Obstet. Gynaecol. Can. 2014, 36, 575–576. [Google Scholar] [CrossRef]
  22. Perry, J. Gait Analysis: Normal and Pathological Function; SLACK: West Deptford, NJ, USA, 2010. [Google Scholar]
  23. Kaufman, K.R.; Sutherland, D.H. Human Walking; Lippencott Williams & Wilkins: Philadelphia, PA, USA, 2006. [Google Scholar]
  24. DeLong, E.R.; DeLong, D.M.; Clarke-Pearson, D.L. Comparing the Areas under Two or More Correlated Receiver Operating Characteristic Curves: A Nonparametric Approach. Biometrics 1988, 44, 837–845. [Google Scholar]
  25. Hanley, J.A.; Hajian-Tilaki, K.O. Sampling Variability of Nonparametric Estimates of the Areas under Receiver Operating Characteristic Curves: An Update. Acad. Radiol. 1997, 4, 49–58. [Google Scholar] [CrossRef]
  26. Sutherland, D.H.; Davids, J.R. Common Gait Abnormalities of the Knee in Cerebral Palsy. Clin. Orthop. Relat. Res. 1993, 288, 139–147. [Google Scholar]
  27. Baumann, J.U.; Ruetsch, H.; Schürmann, K. Distal Hamstring Lengthening in Cerebral Palsy. An Evaluation by Gait Analysis. Int. Orthop. 1980, 3, 305–309. [Google Scholar] [CrossRef]
  28. Crenna, P. Spasticity and “Spastic” Gait in Children with Cerebral Palsy. Neurosci. Biobehav. Rev. 1998, 22, 571–578. [Google Scholar]
  29. Tuzson, A.E.; Granata, K.P.; Abel, M.F. Spastic Velocity Threshold Constrains Functional Performance in Cerebral Palsy. Arch. Phys. Med. Rehabil. 2003, 84, 1363–1368. [Google Scholar]
  30. Perry, J. Newsam, C. Function of the Hamstrings in Cerebral Palsy. In The Diplegic Child: Evaluation and Management; American Academy of Orthopaedic Surgeons: Rosemont, IL, USA, 1992. [Google Scholar]
  31. Fowler, E.G.; Goldberg, E.J. The Effect of Lower Extremity Selective Voluntary Motor Control on Interjoint Coordination during Gait in Children with Spastic Diplegic Cerebral Palsy. Gait Posture 2009, 29, 102–107. [Google Scholar]
  32. Arnold, A.S.; Liu, M.Q.; Schwartz, M.H.; Õunpuu, S.; Dias, L.S.; Delp, S.L. Do the Hamstrings Operate at Increased Muscle–tendon Lengths and Velocities after Surgical Lengthening? J. Biomech. 2006, 39, 1498–1506. [Google Scholar] [CrossRef]
  33. Hicks, J.L.; Delp, S.L.; Schwartz, M.H. Can Biomechanical Variables Predict Improvement in Crouch Gait? Gait Posture 2011, 34, 197–201. [Google Scholar]
  34. Choi, J.Y.; Park, E.S.; Park, D.; Rha, D.-W. Dynamic Spasticity Determines Hamstring Length and Knee Flexion Angle during Gait in Children with Spastic Cerebral Palsy. Gait Posture 2018, 64, 255–259. [Google Scholar] [CrossRef]
  35. Damiano, D.L.; Laws, E.; Carmines, D.V.; Abel, M.F. Relationship of Spasticity to Knee Angular Velocity and Motion during Gait in Cerebral Palsy. Gait Posture 2006, 23, 1–8. [Google Scholar] [CrossRef]
  36. Goldberg, E.J.; Requejo, P.S.; Fowler, E.G. Joint Moment Contributions to Swing Knee Extension Acceleration during Gait in Children with Spastic Hemiplegic Cerebral Palsy. J. Biomech. 2010, 43, 893–899. [Google Scholar] [CrossRef]
  37. Daly, C. Factors Associated with Increased Terminal Swing Knee Flexion in Cerebral Palsy. Gait Posture 2021, 89, 126–131. [Google Scholar] [CrossRef]
  38. Murphy, N.A.; Irwin, M.C.N.; Hoff, C. Intrathecal Baclofen Therapy in Children with Cerebral Palsy: Efficacy and Complications. Arch. Phys. Med. Rehabil. 2002, 83, 1721–1725. [Google Scholar] [CrossRef]
  39. Manikowska, F.; Chen, B.P.; Jóźwiak, M.; Lebiedowska, M.K. Assessment of Selective Motor Control in Clinical Gillette’s Test Using Electromyography. Eur. J. Phys. Rehabil. Med. 2016, 52, 176–185. [Google Scholar]
  40. Miller, F. Cerebral Palsy; Springer Science & Business Media: Berlin/Heidelberg, Germany, 2005; ISBN 9780387271248. [Google Scholar]
  41. McCarthy, J.; Wade Shrader, M.; Graham, K.; Veerkamp, M.; Brower, L.; Chambers, H.; Davids, J.R.; Kay, R.M.; Narayanan, U.; Novacheck, T.F.; et al. Establishing Surgical Indications for Hamstring Lengthening and Femoral Derotational Osteotomy in Ambulatory Children with Cerebral Palsy. J. Child. Orthop. 2020, 14, 50–57. [Google Scholar] [CrossRef]
  42. Mayer, N.H.; Esquenazi, A. Muscle Overactivity and Movement Dysfunction in the Upper Motoneuron Syndrome. Phys. Med. Rehabil. Clin. N. Am. 2003, 14, 855–883. [Google Scholar]
  43. Mohamed, O.; Perry, J.; Hislop, H. Relationship between Wire EMG Activity, Muscle Length, and Torque of the Hamstrings. Clin. Biomech. 2002, 17, 569–579. [Google Scholar]
  44. Onishi, H.; Yagi, R.; Oyama, M.; Akasaka, K.; Ihashi, K.; Handa, Y. EMG-Angle Relationship of the Hamstring Muscles during Maximum Knee Flexion. J. Electromyogr. Kinesiol. 2002, 12, 399–406. [Google Scholar]
  45. Papageorgiou, E.; Simon-Martinez, C.; Molenaers, G.; Ortibus, E.; Van Campenhout, A.; Desloovere, K. Are Spasticity, Weakness, Selectivity, and Passive Range of Motion Related to Gait Deviations in Children with Spastic Cerebral Palsy? A Statistical Parametric Mapping Study. PLoS ONE 2019, 14, e0223363. [Google Scholar] [CrossRef] [Green Version]
Figure 1. Standard popliteal angle (PA) test.
Figure 1. Standard popliteal angle (PA) test.
Applsci 12 09210 g001
Figure 2. Knee flexion angle at the end of the swing phase during walking (Kts).
Figure 2. Knee flexion angle at the end of the swing phase during walking (Kts).
Applsci 12 09210 g002
Figure 3. Knee position at the end of swing/initial stance (Kts) increases with the popliteal angle (PA) according to the equation: Kts = 5.00 + 0.31 × PA (r = 0.39; p < 0.001) in the limbs of patients with CP. Each circle represents the Kts value for the specific PA angle acquired from one single study participant.
Figure 3. Knee position at the end of swing/initial stance (Kts) increases with the popliteal angle (PA) according to the equation: Kts = 5.00 + 0.31 × PA (r = 0.39; p < 0.001) in the limbs of patients with CP. Each circle represents the Kts value for the specific PA angle acquired from one single study participant.
Applsci 12 09210 g003
Figure 4. The results of ROC analysis (AUC = 0.66, p < 0.0001) indicate that the value of Kts = 13.93° generates the cutoff value (sensitivity = 75%, specificity = 51.5%) to detect the absence of knee flexors hypertonia. For Kts ≥ 13.93°, the probability of absence of hypertonia (as detected with TAS at fast velocities HYPvf) decreases.
Figure 4. The results of ROC analysis (AUC = 0.66, p < 0.0001) indicate that the value of Kts = 13.93° generates the cutoff value (sensitivity = 75%, specificity = 51.5%) to detect the absence of knee flexors hypertonia. For Kts ≥ 13.93°, the probability of absence of hypertonia (as detected with TAS at fast velocities HYPvf) decreases.
Applsci 12 09210 g004
Figure 5. The results of ROC analysis (AUC = 0.587, p = 0.022) indicate that the value of popliteal angle (PA = 30°) generates the cutoff value (sensitivity = 89.07%, specificity = 25.44%) to detect the absence of knee flexors hypertonia. For PA ≥ 30°, the probability of absence of hypertonia decreases.
Figure 5. The results of ROC analysis (AUC = 0.587, p = 0.022) indicate that the value of popliteal angle (PA = 30°) generates the cutoff value (sensitivity = 89.07%, specificity = 25.44%) to detect the absence of knee flexors hypertonia. For PA ≥ 30°, the probability of absence of hypertonia decreases.
Applsci 12 09210 g005
Table 1. The popliteal angle values (PA) and knee angular position at the end of swing/initial stance (Kts) were larger in the limbs with clinically detected knee flexors hypertonia, but the differences were not statistically significant for PA when hypertonia had been identified using TAS at slow velocities (HYPvs).
Table 1. The popliteal angle values (PA) and knee angular position at the end of swing/initial stance (Kts) were larger in the limbs with clinically detected knee flexors hypertonia, but the differences were not statistically significant for PA when hypertonia had been identified using TAS at slow velocities (HYPvs).
Absence of Hypertonia (n = 117)Presence of Hypertonia (n = 96)p
Angle (deg)MeanMedianMinMaxSDMeanMedianMinMaxSD
PA39.6640.005.0070.0014.0342.6040.0010.0080.0012.960.23
Kts15.6014.500.5751.819.9920.4019.092.1452.5711.27<0.001
n: number of limbs; SD: standard deviation; bold values denote statistical significance at the p ≤ 0.05 level.
Table 2. The popliteal angle values (PA) and knee angular position at the end of swing/initial stance (Kts) were larger in the limbs with clinically detected knee flexors hypertonia, when hypertonia had been identified using TAS at fast velocities (HYPvf).
Table 2. The popliteal angle values (PA) and knee angular position at the end of swing/initial stance (Kts) were larger in the limbs with clinically detected knee flexors hypertonia, when hypertonia had been identified using TAS at fast velocities (HYPvf).
Absence of Hypertonia (n = 101)Presence of Hypertonia (n = 112)p
Angle (deg)MeanMedianMinMaxSDMeanMedianMinMaxSD
PA38.9640.005.0080.0014.3842.8140.0010.0075.0012.660.05
Kts14.8513.550.5752.419.8920.3918.972.1452.5711.01<0.001
n: number of limbs; SD: standard deviation; bold values denote statistical significance at the p ≤ 0.05 level.
Table 3. The cutoff values of popliteal angle (PA) and knee angle at the end of swing/initial stance (Kts) during gait to detect the presence of knee flexors hypertonia based on two clinical tests: TAS at slow (HYPvs) and TAS fast (HYPvf) velocities.
Table 3. The cutoff values of popliteal angle (PA) and knee angle at the end of swing/initial stance (Kts) during gait to detect the presence of knee flexors hypertonia based on two clinical tests: TAS at slow (HYPvs) and TAS fast (HYPvf) velocities.
AUCCutoff
(deg)
Sensitivity
(%)
Specificity
(%)
p
Kts (HYPvs)0.64116.6861.4664.960.000395
Kts (HYPvf)0.66013.9375.0051.480.000055
PA (HYPvs)0.56230.0090.2024.430.102084
PA (HYPvf)0.58730.0089.0825.440.021889
The strength of the impact was evaluated with the area under the sensitivity/specificity curve (AUC) where 1 means the strongest and 0.5 no impact with a statistical significance of the p-value. Bold values denote statistical significance at the p ≤ 0.05 level.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Manikowska, F.; Brazevič, S.; Jóźwiak, M.; Lebiedowska, M.K. The Role of Knee Flexors Hypertonia in the Decision-Making of Hamstring Lengthening Surgery for Individuals with Cerebral Palsy. Appl. Sci. 2022, 12, 9210. https://doi.org/10.3390/app12189210

AMA Style

Manikowska F, Brazevič S, Jóźwiak M, Lebiedowska MK. The Role of Knee Flexors Hypertonia in the Decision-Making of Hamstring Lengthening Surgery for Individuals with Cerebral Palsy. Applied Sciences. 2022; 12(18):9210. https://doi.org/10.3390/app12189210

Chicago/Turabian Style

Manikowska, Faustyna, Sabina Brazevič, Marek Jóźwiak, and Maria K. Lebiedowska. 2022. "The Role of Knee Flexors Hypertonia in the Decision-Making of Hamstring Lengthening Surgery for Individuals with Cerebral Palsy" Applied Sciences 12, no. 18: 9210. https://doi.org/10.3390/app12189210

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop