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SYSTEMATIC REVIEWS

Differentiating Between Idiopathic Toe Walking and Cerebral Palsy

A Systematic Review

Schlough, Kathleen PT, DSc, PCS; Andre, Kerryn PT, DPT; Owen, Marley PT, DPT; Adelstein, Lindsey PT, DPT; Hartford, Mary Claire PT, DPT; Javier, Bernadette PT, DPT; Kern, Rachel PT, DPT

Author Information
doi: 10.1097/PEP.0000000000000659
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INTRODUCTION

Toe walking is defined as the absence or inability to obtain heel strike at initial contact and during the stance phase of walking.1 Variability in walking pattern during development is considered typical; however, a consistent toe walking pattern after the age of 3 years is considered atypical.2 A small cross-sectional study found the prevalence of idiopathic toe walking (ITW) to be approximately 1 in 20 children.3 ITW is a medical diagnosis of exclusion of other musculoskeletal or neurological conditions.4 These diagnoses can include forms of cerebral palsy (CP), sensory processing disorder, autism spectrum disorder, muscular dystrophy, or spina bifida.4 Toe walking of known sensory origin has been excluded from this study secondary to its more unique presentation.

ITW, a medical diagnosis given when there is an inability to establish a cause for habitual toe walking, is diagnosed via exclusion; however, there are several characteristics of ITW that assist clinicians in identifying this condition. Motion restriction at the ankle is one of the most common indicators for an ITW diagnosis in the pediatric population.4 Upon request to heel walk, a child with a diagnosis of ITW, according to a study by Pomarino et al,4 will be unable to heel walk or will heel walk with biomechanical compensations. When requested to walk with their feet flat on the ground, only 17% of the participants diagnosed with ITW were able to do so.4 Participants with ITW present with difficulty during postural tasks, such as standing and walking, and can often have trouble with coordination of movement.5

Participants with ITW often have similar characteristics to participants mild spastic diplegia (MSD), a type of CP in which the lower extremities are more affected than the upper extremities. CP is defined as a “group of permanent disorders of the development of movement and posture, causing activity limitation, that are attributed to non-progressive disturbances that occurred in the developing fetal or infant brain. The motor disorders of CP are often accompanied by disturbances of sensation, perception, cognition, communication, and behaviour, by epilepsy, and by secondary musculoskeletal problems.”6 The prevalence of CP is 2.1 per 1000 live births, according to a meta-analysis by Oskoui et al,7 making CP the most common movement disorder in children. Participants with CP often present with atypical movement patterns, muscle weakness, changes in muscle tone, spasticity, and impaired selective motor control. A diagnosis of CP typically accompanies deficits in functional mobility, force production, and the ability to fractionate movement.8 Neurological symptoms including spasticity, ataxia, and athetosis are identifiable in moderate to severe cases of CP. In more mild cases, such as MSD, symptoms may only become apparent during observation of movement.

It is difficult to differentiate between ITW and mild CP due to similarities in walking patterns. However, using standardized examination procedures, participants can be classified beyond their medical diagnosis. The authors conducted this systematic review to determine the evidence-based examination procedures needed to establish a movement system diagnosis to assist clinicians in distinguishing between the 2 patient populations. The authors included each examination procedure that appeared in more than one article. Although physical therapists do not establish these medical diagnoses, clinicians determine movement system diagnoses based on established tests of impairments and analysis of functional tasks.8

Scheets et al8 proposed a system of 9 movement system diagnoses for individuals with neuromuscular conditions that was developed based on clinician experience in combination with standardized clinical examination. These include movement pattern coordination deficit, force production deficit, fractionated movement deficit, postural vertical deficit, sensory selection and weighting deficit, sensory detection deficit, hypokinesia, dysmetria, and cognitive deficit. According to the APTA,9 a movement system is “the term used to represent the collection of systems (cardiovascular, pulmonary, endocrine, integumentary, nervous, and musculoskeletal) that interact to move the body or its component parts.” A movement system diagnosis is determined by a physical therapist to maximize an individual's functional potential.8 A movement system diagnosis is a clinician-given categorization that describes the persons' primary problem based on their clinical presentation. In the context of this review, the authors determined that fractionated movement deficit is often observed in participants with CP and movement pattern coordination deficit is often observed in participants with ITW. Because participants with CP by definition have an upper motor neuron lesion that makes isolated joint movement more difficult,6 a fractionated movement deficit is the most appropriate movement system diagnosis. Participants with ITW present with a varying walking pattern with ability to produce typical kinematics.10 Therefore, a movement pattern coordination deficit, in accordance with the definition by Scheets et al,8 was determined by the authors to be the most appropriate.

According to Scheets et al,8 the primary problem associated with movement pattern coordination deficit is, “the inability to coordinate an intersegmental task because of a deficit in timing and sequencing of one segment in relation to another. The movement dysfunction in the lower extremity is primarily observed during postural control tasks.” During walking, Scheets et al8 note, “variable foot placement or line of progression or may be guarded with slow, small steps.”

Scheets et al8 define fractionated movement deficit as: “the inability to fractionate movement associated with moderate or greater hyperexcitability. [It] may describe the upper extremity, lower extremity, or both. Always associated with central neurological deficit.” To diagnose a child with a fractionated movement deficit, a clinician should examine the child's ability to fractionate movement and generate force rapidly.8 A measurement of muscle tone, identification of reflexes present, and performance of a task analysis to assess for the ability to isolate movement should also be included in the physical examination.8

Movement system diagnoses are established by compiling data from the history, physical examination at the level of body structure and function, and task analysis at the level of activity according to the World Health Organization's International Classification of Functioning, Disability and Health model (ICF).11 For example, Scheets et al8 report that a movement system diagnosis of fractionated movement deficit may be given to individuals who present with the following body structure and function-level impairments: inability to fractionate movement, inability to make rapid reversals in movement, inability to generate force rapidly, and/or grade 3 to 4 on the Modified Ashworth Scale. With task analysis at the level of activity limitation, an individual with a fractionated movement deficit may demonstrate characteristic findings during floor to stand or sit to stand.

The ICF model,11 body structure and function, activity limitation, and participation restriction identification, allows therapists to identify movement variables and therefore to classify each person's presentation. Clinicians then match each person's specific problem with appropriate physical therapy intervention. Medical diagnoses are not sufficient to direct specific physical therapy intervention, but with a targeted plan of care guided by movement system diagnoses, therapists are able to provide more efficient treatments for each patient.

The purpose of this systematic review is to identify examination components that enable a clinician to distinguish between participants with ITW and CP to accurately categorize them into their respective movement system diagnosis of movement pattern coordination deficit or fractionated movement deficit.

METHODS

Search Strategies

A comprehensive search strategy of multiple databases was used including PubMed, CINAHL, SPORTDiscus, and Medline. The authors conducted their initial search in September 2016. A follow-up literature search following the same strategy was completed in June 2019. There was no limit placed on publication date. Search was limited to publications written in English. Gray literature and publications excluded from the above databases were not assessed. Authors identified appropriate search terms prior to initiating the search. Search terms used include idiopathic toe walking and cerebral palsy, idiopathic toe walking and spastic diplegia, habitual toe walking and cerebral palsy, and habitual toe walking and spastic diplegia.

Eligibility Criteria

Studies were eligible if they included participants diagnosed with ITW and CP, measured body structures and functions, or analyzed tasks at the level of activity. Inclusion criteria were (1) a diagnosis of ITW or CP, (2) between the ages of 2 and 18 years, and (3) no comorbid conditions previously identified to cause toe walking. Exclusion criteria were articles that (1) primarily discussed physical therapy intervention for ITW or CP and (2) primarily discussed medical intervention for ITW or CP.

Operational Definitions

The definition of ITW was the absence of heel strike at initial contact and stance phase during walking.1 CP was referred to as a medical cerebral palsy diagnosis, which is to be differentiated from a specific MSD diagnosis. A specific MSD diagnosis is defined as mild lower extremity involvement that may include common neurological signs of CP.11

Examination of body structure and function referred to measurements of range of motion, flexibility, and spasticity. Range of motion was of ankle dorsiflexion, which was performed in the supine position with the knee extended using a goniometer. Flexibility was measurement of the popliteal angle via the 90/90 test in the supine position with the hip flexed to 90°. Spasticity was measured with the Modified Ashworth Scale. Examination of activity-level testing referred to walking analysis, which included observation of kinematic patterns, muscle activation, and spatial temporal variables. Electromyography (EMG) was defined as a tool used during lower extremity exercise and walking analysis to examine patterns of muscle activity during static and dynamic tasks. Static EMG was a measurement of differences in obligatory coactivation during voluntary contraction of the quadriceps and gastrocnemius, such as firing of musculature during both resisted knee extension and isometric quadriceps sets. Dynamic EMG activity was analyzed as the percentage of the walking cycle in relation to the onset and termination of muscle activity while walking, specifically the gastrocnemius, quadriceps, and tibialis anterior.

Selection of Studies

Two investigators independently screened titles and abstracts. Based on the abstracts, the investigators obtained copies of potential articles to determine eligibility for inclusion. After the preliminary search, article titles were screened for duplicates and topic relevance. Articles were excluded if the article analyzed walking of participants diagnosed with ITW only, the article primarily discussed medical interventions, the article primarily reviewed physical therapy interventions, and duplicate articles. Abstracts of the remaining studies were screened by 2 reviewers. Of those screened, a select number of articles were chosen for appraisal based on agreement of yes/no consensus for potential to meet eligibility criteria, and full-text copies were retrieved. There was no discrepancy in yes/no consensus between reviewers for determining eligibility. All studies were cross-sectional or retrospective cohort designs, with a level of evidence of 3 on the Oxford Center for Evidence-Based Medicine.12 Systematic reviews were not found during the search process that met the eligibility criteria (Figure).

Fig
Fig:
Article selection. (A) Flowchart of initial article selection through September 2016. (B) Flowchart of additional relevant articles identified through June 2019.

Data Extraction

Body structure and function variables were extracted if they appeared in 2 or more articles selected for inclusion in this article. Data were extracted if they were categorized as body structure and function and activity limitation, as defined by the ICF11 model.

RESULTS

Participants

There were 140 participants in total that were included in the systematic review. Sample sizes ranged from 14 to 45 participants (Table 1). The participants for each study were separated into either ITW or CP groups. The age of the participants ranged from 2 to 16 years.

TABLE 1
TABLE 1:
Summary of Studies

Body Structures and Functions and Activity Limitations Studied

The included studies evaluated the differences between many variables in the body structure and function and activity limitation levels of the ICF11 model. The studies investigated objective body structure and function measurements—range of motion, flexibility, spasticity, and EMG, as well as activity level testing including walking analysis, to compare and contrast presentations of those with ITW and those with CP (Table 1).

Analysis of the Evidence

A meta-analysis was not conducted secondary to poor homogeneity between studies as well as lack of availability of effect size calculation for variables. Effect size was calculated for each variable between ITW and CP groups. Table 2 contains results classified by components of the ICF model that were analyzed. Effect size, via Cohen's suggested interpretation,18 allowed quantification of the magnitude of the difference between groups when available. Effect size was calculated using Cohen's d. Pooled standard deviation was calculated. ITW was group 1 and CP was group 2 for each study and, therefore, a negative effect size indicated that the mean for the CP group was larger.18 Walking speed and ankle dorsiflexion range of motion were the 2 measures compared that had an effect size smaller than 0.8, but many of the studies did not include means and/or standard deviations. Other measures in which effect size could be calculated were large effect sizes, signifying a large difference between the ITW and CP groups.

TABLE 2
TABLE 2:
Effect Sizes Between ITW and CP Groups

Examination of Body Structure and Function

Range of Motion and Flexibility/Muscle Length

The 6 studies2,13–17 commented on the passive dorsiflexion range-of-motion differences between CP and ITW groups. In 5 of the 6 studies, dorsiflexion range of motion was noted to be tested in the supine position with the knee extended using a goniometer. Haynes et al13 did not specify method for obtaining dorsiflexion range of motion but did note that inability to attain neutral dorsiflexion was considered an ankle contracture. Rose et al17 and Policy et al16 reported that, although CP and ITW groups both have decreased dorsiflexion range of motion, the deficit was not clinically or significantly different between the groups. Kelly et al2 reported that both groups had limited passive range of motion into dorsiflexion, although there were no comments on clinical or statistical significance. Kalen et al15 commented only on the ITW group, reporting these participants have limited dorsiflexion range of motion, but did not comment on clinical or statistical significance. Hicks et al14 reported that participants with CP did not have “heel cord contractures” and some of the ITW group participants had decreased passive range of motion, but they did not comment on the significance of these differences. Haynes et al13 reported that more participants with ITW than CP had ankle contractures. The presence of an ankle contracture did not differentiate between the 2 groups. We found no significant differences in dorsiflexion range of motion between the 2 diagnoses.

Rose et al,17 Hicks et al,14 and Policy et al16 reported on the differences between popliteal angle in the 2 groups. Popliteal angle was measured via the 90/90 test in the supine position with the hip flexed to 90°. The groups with CP had increased popliteal angles, indicating greater hamstring tightness, with little to no increase in popliteal angle in the ITW groups.14,16,17 Rose et al17 and Policy et al16 reported statistical significance between the 2 groups; however, Hicks et al14 did not comment on clinical or statistical significance. There were large effect sizes, but values overlapped between the 2 groups, suggesting some similarity in hamstring length between the groups. This review concluded that participants with CP have significantly increased popliteal angles, indicated hamstring tightness.

Muscle Spasticity

The Modified Ashworth Scale was used to classify muscle spasticity to differentiate between the 2 diagnoses in 2 of the 3 articles that noted changes in spasticity. Two studies16,17 reported an increase in muscle spasticity in the gastrocnemius on the Modified Ashworth Scale with CP compared with ITW, reported as a statistically significant difference. Haynes et al13 commented on upper motor neuron signs as a group, including spasticity, but did not specify method of evaluation. Haynes et al13 reported an increase in prevalence of these signs in CP as compared with ITW. An increase in muscle spasticity was seen in CP as compared with ITW.

Static EMG Analysis

Two studies16,17 measured differences in obligatory coactivation during voluntary contraction of quadriceps and gastrocnemius to differentiate between the 2 diagnoses.16,17 Rose et al17 had participants sit unsupported on an examination table, while dorsiflexing the foot and extending the leg, on a randomly selected leg, for 2 seconds. Participants were instructed to extend the knee to −25° of flexion and hold against resistance. Similarly, Policy et al16 obtained static coactivation by asking the participant to extend the leg to a −30° angle of knee flexion while dorsiflexing the foot, holding against resistance for 5 seconds for a total of 3 trials. Policy et al16 reported coactivation during seated knee extension and plantarflexion using the same criteria for measurement. Duration of coactivation of the gastrocnemius during both seated resisted knee extension and a quadriceps set was significantly increased in participants with CP compared with participants with ITW.16,17 During voluntary plantarflexion, coactivation of the quadriceps muscles was not significantly different between the 2 groups. Participants with CP demonstrate coactivation of the quadriceps and gastrocnemius unlike participants with ITW.

Activity-Level Examination

Walking Analysis and Dynamic EMG

Walking analysis and movement-based observation provided relevant information on kinematic patterns for both ITW and CP participants. Data were collected through walking velocity and sagittal plane kinematics of typical heel-toe walking,14,15 or through having control groups toe walk and compare between participants with ITW and CP.2,15,17

Both diagnoses had plantarflexion and lacked the first heel-rocker at initial contact. Participants with ITW actively contracted their gastrocnemius earlier in swing phase. Hicks et al14 found that participants with CP had a progressive excursion toward dorsiflexion in swing phase but struck the ground for the next walking cycle with the midfoot to forefoot. This is confirmed with EMG analysis of the gastrocnemius by Rose et al17 and Policy et al16 with later activation of the gastrocnemius during swing phase for participants with CP versus participants with ITW; however, both diagnoses had premature firing of the gastrocnemius during swing.16,17 Kalen et al15 reported no significant differences in onset or cessation of gastrocnemius firing between participants with ITW and CP.15

In Kelly et al2 and Hicks et al,14 participants with ITW had typical kinematics at the knee whereas participants with CP did not. Kelly et al2 reported that participants with ITW had maximal knee extension at initial contact, indicative of typical knee joint motion. Some participants with ITW had atypical knee kinematics with knee hyperextension during stance.14 Participants with CP maintained knee flexion upon initial contact and did not reach maximal knee extension until mid or late stance.2

Kelly et al2 and Hicks et al14 identified that participants with ITW frequently had typical kinematics at the hip whereas participants with CP did not. Participants with CP often exhibited increased hip flexion throughout the walking cycle.14

Spatial temporal variables were measured in the studies by Kelly et al2 and Rose et al.17 Kelly et al2 reported no difference in speed, cadence, or stride length, while Rose et al17 commented on only walking speed. CP and ITW groups had decreased speed, with ITW demonstrating slower overall walking speed but without significant differences.17

Participants with ITW had variable kinematics throughout walking, alternating between heel-striking and toe-striking whereas participants with CP had similar kinematics that are present with repetitive and predictable walking cycles.14 Despite differences in cocontraction during static testing, there were no significant differences in muscular coactivation during walking when comparing CP and ITW groups.16

Participants with ITW had atypical sagittal plane walking kinematics at the ankle with typical kinematics at the knee and hip. Participants with CP had atypical sagittal plane kinematics at the ankle, knee, and hip. Although both groups had atypical kinematics at the ankle, ankle position during swing phase differed between the 2 groups.

SUMMARY

Findings from an examination of body structure and functions and activity limitations help pinpoint key characteristics in differentiating between CP and ITW. Through clinical examination, individuals with CP had spasticity (presence of an upper motor neuron sign), increased hamstring tightness, and increased coactivation of the gastrocnemius muscle during resisted seated knee extension and quadriceps set. No significant differences were noted between the 2 diagnoses in dorsiflexion range of motion, but there was a significant difference in hamstring.

Walking was assessed with movement-based observations and EMG analysis. Participants with ITW had typical hip and knee kinematics during walking. Participants with CP had increased hip flexion during all phases of walking and maintained knee flexion during initial contact in stance. Individuals with CP also had active dorsiflexion during swing phase but struck the ground in midfoot or forefoot stance during initial contact concurrent with their atypical knee kinematics. Participants with ITW had active plantarflexion during swing, striking the ground in midfoot or forefoot stance during initial contact with typical knee kinematics. Participants with ITW had more variability in walking kinematics between trials. No differences were noted in spatial-temporal variables between the 2 diagnoses; however, a decrease in walking speed was noted for both diagnoses. There were no differences between muscle coactivation during walking.

DISCUSSION

The purpose of this systematic review is to determine the most essential examination findings pertinent to differentiating between CP (MSD) and ITW based on the current literature. Due to their similar characteristics, it is recommended that a movement system diagnosis approach be used to classify results for more targeted plan of care.

A child with CP has characteristics classifying the child with a diagnosis of “fractionated movement deficit.” In the studies in this review, the participants with CP were unable to fractionate movement as evidenced by cocontraction during resisted knee extension and quadriceps set, as well as atypical hip and knee kinematics during walking. Although less obvious in the classification process, children with ITW had characteristics of “movement pattern coordination deficit.” Participants with ITW had the ability to fractionate movement against gravity (lacked cocontraction with resisted knee extension) and did not have increased spasticity. Participants with ITW had variable walking kinematics including alternating between heel-striking and toe-striking.14

We recommend assessing a child's hamstring length via the 90/90 test, spasticity and muscle coactivation during resisted knee extension and quadriceps set to differentiate between the 2 diagnoses. Task analysis should include, but not be limited to, analysis of walking and other functional tasks, including variability of movement. During walking analysis, we recommend observing ankle, knee, and hip kinematics in the sagittal plane. More specifically, knee and hip position during stance and swing phases of walking should be compared with typical movement patterns to differentiate between groups. Electromyographic analysis during walking is not recommended to differentiate between the diagnoses. Dorsiflexion range of motion should not be used to differentiate between the 2 diagnoses; however, all components of physical therapy examination should be performed to assess the unique characteristics of each child's characteristics.

Impaired selective motor control yielding atypical muscular cocontraction via palpation, the presence of spasticity, and significantly decreased hamstring length results in a movement system diagnosis of fractionated movement deficit, secondary to upper motor neuron involvement associated with CP. In combination with the deficits listed earlier, decreased hamstring length in these participants is an orthopedic manifestation partially from neurologic causes.19 In contrast, an examination finding of increased variability in foot position during walking and typical selective motor control, evidenced by a lack of cocontraction, as well as less severe hamstring tightness, results in a movement system diagnosis of movement pattern coordination deficit, secondary to an intact neurological system.

Clinical Implications

Using the recommended tests and measures during an examination yields accurate movement system diagnosis classification and a targeted plan of care. A movement pattern coordination deficit diagnosis is the result of difficulty with coordination of intersegmental motor tasks, which typically improves with practice and instruction via neuromuscular reeducation. In contrast, a fractionated movement deficit diagnosis is a result of poor selective motor control and indicates interventions that promote increased selective movement. Without addressing impaired selective motor control when treating children with fractionated movement deficit, progress will be limited.

Specific treatments are more effective based on the primary problem. For example, Goldberg et al20 reported that hamstring lengthening did not always increase stride length in children with CP. Because these children had poor selective control, it was difficult for them to isolate their knee extensors while in hip flexion during the swing phase of walking.20 While in hip flexion, the knee was more likely to be flexed, instead of extended, secondary to the upper motor neuron lesion that results in overall movement patterns classically referred to as flexor and extensor synergies.20 Therefore, despite lengthening a tight hamstring muscle, children had continued knee flexion during swing phase.20 Selective motor control should be measured via seated knee extension or a quadriceps set for a child with toe-walking before initiating intervention. Similarly, selective motor control needs to be examined when considering serial casting at the ankle as an intervention strategy.21

Effectiveness of treatment is dependent on a thorough and accurate examination process. Treatment is best guided by movement system diagnosis. The purpose of this review is not to recommend specific interventions, but rather to suggest that differentiating between the 2 diagnoses allows more targeted treatment.

Research Recommendations

Additional research is needed to more accurately distinguish between the 2 populations. Future research should include rigorous study designs with homogenous participant groups. Groupings could be determined by medical diagnosis and severity and by movement system diagnosis. Further research is needed on activity limitation and participation restriction.

Limitations

Articles in this review were 20 years and older, secondary to a lack of current research in this area. Most included studies did not examine the same defined variables. Further conclusions could have been made if the same variables had been used in all studies. Diagnostic criteria for ITW were not clearly defined, which may have contributed to variability in participant characteristics. None of the studies measured differences in strength.

CONCLUSION

A physical therapist should complete an examination consisting of components of the ICF model to determine clinical differences between ITW and CP. Performing and interpreting the examination components discussed in this review allows clinicians to accurately determine the primary functional limitation and classify children into their appropriate movement system diagnosis.

ACKNOWLEDGMENTS

This article is dedicated to the memory of Kathleen Schlough and her passion and dedication to the field of pediatric physical therapy. The authors would like to thank Deborah King, PhD, and Rumit Singh Kakar, PT, PhD, for their contributions to this article.

REFERENCES

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Keywords:

cerebral palsy; diagnostic; fractionated movement deficit; idiopathic toe walking; mild spastic diplegia; movement pattern coordination deficit; movement system diagnosis; systematic review; toe walking; walking; walking analysis

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