Caudill, Angela MPT; Flanagan, Ann PT, PCS; Hassani, Sahar MS; Graf, Adam MS; Bajorunaite, Ruta PhD; Harris, Gerald PhD; Smith, Peter MD
Osteogenesis imperfecta (OI) is a heritable connective tissue disorder characterized by bone fragility, decreased bone mineral density, fractures, and skeletal deformities. The incidence of OI is 1 in 5000 to 10000 individuals.1 In most cases, OI is caused by quantitative and qualitative defects of type I collagen fibers.1 There is variability in expression of OI with musculoskeletal manifestations ranging from mild to severe. Sillence et al2 devised a classification scheme in 1979, dividing OI into 4 types on the basis of inheritance, radiological findings, and clinical examination. Twenty years later, through research and development, new types and variants have been identified and include at least 8 different types of OI.3
The mildest and most common form of OI is type I, with clinical manifestations including recurrent fractures due to osteopenia, normal or near normal stature, blue sclera, hearing loss, dentinogenesis imperfecta, weakness, and joint laxity.3 Individuals with type I OI are generally community ambulators who may experience limitations in overall strength, walking, running, daily living activities, and keeping up with peers.4,5 Children with type I OI often experience their first fracture between 6 months and 2 years of age, corresponding with the start of mobility and ambulation.3 Frequency of fractures is usually less than 2 per year with fractures mainly occurring in the diaphysis of long bones.3 Fractures typically decrease progressively after puberty.3
Following a fracture, activities of daily living are limited due to immobilization or corrective orthopedic surgery or both. As expected, children report pain at the time of fracture and during the healing time, which reduces their activity level.6 Increased fatigue, decreased functional ability, and decreased physical fitness in children with OI have been reported. Van Brussel et al7 reported that a 3-month standardized fitness training program consisting of basic functional exercises can significantly increase aerobic performance and muscle strength, tending to decrease fatigue in children with types I and IV OI. Post fracture, muscles and bones become weaker with greater susceptibility to refracture. This experience can delay motor skill development and cause acquired motor skills to regress and interfere with overall function. Preventing this cyclical pattern from occurring has been challenging for the clinician, although surgical intervention, such as rodding, and bisphosphonates have helped these children stay more active and healthy.8–11
Current treatment includes a combination of modern surgical, medical, and rehabilitative therapies. The overall goal of treatment is to reduce fractures, improve strength, and maximize function. Over the past decade, research has reported the positive effects of pamidronate treatment in improving bone density and preventing skeletal fractures in children with OI.8–13 Land et al8 reported that bisphosphonate treatment improved mobility, ambulation level, and muscle force in children with moderate to severe OI. A study by Sakkers et al14 reported no effects on functional outcomes but did note a reduction in fracture risk of the long bones. DiMeglio and Peacock15 compared oral alendronate and intravenous pamidronate in children with OI and noted improvement in lumbar spine bone mineral density and decreases in fracture incidence in both groups.
Physical therapy plays an important role in helping children to recover from fractures, increase strength, and achieve their performance goals. Although most children with type I OI would benefit from some type of rehabilitation program, many clinicians are unclear regarding the physical limitations of these children.16–18 For fear of fracture, parents or clinicians or both may be too restrictive with the child.19 To improve care for these children, caregivers must understand a child's level of impairment and the resulting effect upon his or her daily life.20
Engelbert et al21,22 evaluated changes in impairments of children with OI, including range of motion, muscle strength, and functional ability, over 1- and 4-year periods, noting that specific impairments did not change over time but rather functional abilities did improve.21,22 The Pediatric Evaluation of Disability Inventory was used by Engelbert et al4 to determine whether the severity of OI might have an influence on functional outcomes.4 It was determined that there was not a significant difference between children with different types of OI in the self-care domain. In the mobility domain, scores varied between children with all types of OI. Social function scores were within the normal range for all children with any type of OI. In children with OI types III and IV, Engelbert22 states that changes in functional ability seem to be restricted, possibly because of a ceiling effect of the disease. He concluded that treatment strategies should focus primarily on improving functional ability than on specific impairments.22
Similar studies have looked at impairment and functional activities as they relate to ankle plantar flexor strength in children with cerebral palsy (CP). In previous studies, children with CP were involved in ankle plantar flexor strengthening home programs.23–25 All children with CP demonstrated increases in ankle plantar flexor strength following a strengthening program; however, there was limited carryover into functional activities. The benefits gained by these children included improved perceptions of strength, flexibility, posture, walking, and the ability to negotiate stairs.24 In addition, psychological benefits of increased well-being and improved participation in school and leisure activities were noted.24 However, in a second study Dodd et al25 reported a trend for improved strength following a 6-week home strengthening program as well as positive trends for improved walking, running, jumping, and stair climbing.
Currently, no studies were found that have examined ankle plantar flexor strength in children with type I OI. This muscle group is important for walking speed and higher-level gross motor skills such as jumping, hopping, stair negotiation, running, and sports activities. The purpose of this study was to determine whether children with type I OI exhibit decreased ankle plantar flexor strength and whether this correlates with their physical function and level of ambulation. On the basis of the International Classification of Functioning, Disability and Health Model, a better understanding of the impairments, activity limitations, and participation restrictions experienced by children with type I OI may allow more directed therapies to improve strength and overall function.
This institutional review board approved study included 20 children with type I OI (“OI group,” aged 6-18 years, 11 boys, 9 girls, mean age = 12.4, SD = 3.6) and an age- and gender-matched group of 20 children who were developing typically (“control group,” aged 6-17 years, 11 boys, 9 girls, mean age = 12.6, SD = 3.7). A parent of each child provided informed consent to participate. If the child was between the ages of 7 and 13 years, an assent from the child was also obtained. Inclusion criteria included a diagnosis of type I OI, between the ages of 5 and 18 years, no surgery in the past 12 months, and the ability to ambulate without an assistive device. All children were community ambulators and could negotiate obstacles independently or with minimal assistance.
The most recent fracture for a subject in the OI group was a nondisplaced tibia fracture 3.5 months prior to participation. An average of 14.8 months had elapsed between a subject's most recent fracture and participation in the study. Within the year prior to testing, 45% of the subjects in the OI group had experienced upper or lower extremity fractures or both. Two years prior to participation, 20 fractures were reported in upper and/or lower extremities as well as 1 cervical fracture. Eight of the 20 subjects in the OI group were receiving bisphosphonate treatment.
Muscle Strength Measures
A physical examination was performed on the lower extremities of each subject by a physical therapist. Two measures of ankle plantar flexor strength were taken using an easy and economical test, the heel-rise test, and a more specific isometric ankle strength test on the Biodex System 3 Dynamometer (Biodex Medical Systems Inc, Shirley, New York) that would result in a precise numerical measurement.
The heel-rise test, described by Daniels and Worthingham,26 rates ankle plantar flexor strength from 0 to 5 according to the number of heel rises the subject is able to complete. Performance of 20 repetitions corresponds to a maximum score of 5, whereas a score of 2 corresponds to full range of antigravity ankle plantar flexion motion (Table 1). Lunsford and Perry27 studied adults ranging in age from 20 to 59 years and recommended 25 standing heel-rise repetitions as the standard for a score of 5. As 25 repetitions may be the suggested number of heel rises needed for adults to score a 5, we continued with the Daniels and Worthingham's published criteria, as our subjects were children and adolescents. Currently, there are no published norms for using the heel-rise test in 6- to 18-year-old children and adolescents.
Bilateral ankle plantar flexor and dorsiflexor isometric strength was assessed on the Biodex System 3 Dynamometer. The child was seated in an upright position with the knee flexed 20° to 30° and the ankle in 10° of plantar flexion. Three trials of maximum isometric strength were collected per limb. The average peak torque was noted from the 3 isometric muscle contractions and normalized to body weight (N m/kg). Because of bone fragility, additional muscle groups were not tested on the Biodex System 3 Dynamometer.
Outcome Assessment Tools
Two outcome assessment questionnaires were completed by a parent: (1) the Pediatric Outcomes Data Collection Instrument (PODCI) and (2) the Gillette Functional Assessment Questionnaire (FAQ). The PODCI included 4 functional assessment scores (upper-extremity functioning, transfers and basic mobility, sports and physical function, and comfort/pain) and a global function score (the average of the 4 functional assessment scores).28,29 Validity of the PODCI was demonstrated by Haynes and Sullivan28 following administration of the questionnaire to 57 children and 27 adolescents who were developing typically. From these data, it is reported that any child scoring in the low 80s or less is functioning at a different level than a child or adolescent who is developing typically.
The FAQ is divided into 3 subscales. The validated walking subscale I describes the child's typical walking ability and rates it on a scale of 1 to 10.30 Subscale II identifies limitations in a child's walking ability. Higher-level functional skills were assessed in subscale III in which parents were asked to rate their child's performance in a variety of gross motor activities as “easy,” “a little hard,” “very hard,” “can't do at all,” or “too young for the activity.” Total scores for each subscale were calculated. Although subscales II and III are not validated, the scores are reported because they were felt to be a good representation of higher-level skills that children who are developing typically, and aged 6 to 18 years, should be capable of performing. Subscale III on the FAQ can also identify higher-level gross motor skills that may be difficult for some children with type I OI and can identify specific areas of focus for physical therapy treatment programs.
Each child completed a Faces Pain Scale-–Revised (FPS-R) on the day they were tested.31 At the time of testing, the child rated their pain from 0 (no pain) to 10 (most severe pain) by identifying the face that showed how much they were hurting.
Descriptive statistics were used to summarize the data. A nonparametric, paired sample signed rank test was used to compare ankle plantar flexion and dorsiflexion strength between the subjects in the OI and control groups. The Spearman correlation coefficient was used to quantify the relationship between the results of the heel-rise test and the isometric strength test of the ankle. A similar method was employed to explore the correlation between ankle plantar flexion/dorsiflexion and a variety of outcome measures. Statistical significance was set at an α level of 0.05. All data were analyzed with SAS version 9.1 software (SAS Institute Inc, Cary, North Carolina).
Strength assessment with the heel-rise test revealed that strength differences were present in the ankle plantar flexors between the subjects in the OI group and control group. All subjects in the control group, between the ages of 6 and 18 years, were able to complete 20 heel rises for a score of 5. Half of the subjects' ankles in the OI group scored a 5 on the heel-rise test. Eleven ankles from the subjects in the OI group scored a 3 to 4 on the heel-rise test with the remaining 9 ankles scoring 2.5 or less. There was no statistically significant difference in ankle plantar flexor strength (P > .05) between the left and right sides in either group or between the 2 groups; however, the mean plantar flexor strength for those in the OI group (3.9 ± 1.2) was lower than the mean for those in the control group (5.0 ± 0).
Of the 20 children with OI, a total of 35 of 40 ankles were evaluated with isometric strength testing on the Biodex System 3 Dynamometer. Three female ankles and 2 male ankles from the OI group were not tested on the system because of discomfort when placed in the apparatus and fear of a fracture occurring. The ankles of these children were removed from the data analysis. All 20 subjects in the control group were evaluated on the Biodex System 3 Dynamometer for a total of 40 ankles. Within the OI and control groups, the subjects had no significant difference in plantar flexion or dorsiflexion strength between the left and right ankles (Table 2). The subjects in the control group had a higher plantar flexion strength for both the left and the right ankle (103.9 ± 42.0 N m/kg and 99.5 ± 40.3 N m/kg, respectively) when compared with the subjects in the OI group (80.8 ± 38.4 N m/kg and 79.1 ± 35.5 N m/kg, respectively). However, these differences failed to reach statistical significance. Ankle dorsiflexion strength was very similar between the 2 groups of children and adolescents with the OI group scoring 45.9 ± 15.6 N m/kg as compared with 45.5 ± 10.1 N m/kg scored by the control group.
To further evaluate the Biodex strength and heel-rise test scores, concurrent validity was determined showing a positive correlation between the heel-rise test score and ankle plantar flexor isometric strength values (r = 0.6, P = .04). Both measures revealed that the subjects in the OI group had decreased plantar flexor strength compared with the subjects in the control group.
Subscales of the PODCI were evaluated, with a maximum subscore of 100. The OI group scored close to the published norms of middle to high 90s as reported by Haynes and Sullivan28 for upper extremity and physical function (mean = 95, SD = 6) and transfers and basic mobility (mean = 96, SD = 6). However, sports and physical function (mean = 66, SD = 23), pain and comfort (mean = 71, SD = 27), and global function and symptoms (mean = 80, SD = 18) scores were all lower than the published norms (Table 3). There was a marginally significant correlation between the sports and physical function and global function subscales with ankle isometric plantar flexion strength as assessed on the Biodex System 3 dynamometer (r = 0.5, P = .05 and r = 0.5, P = .06, respectively). However, dorsiflexion did significantly correlate with these 2 subscales of the PODCI (r = 0.5, P < .01, and r = 0.6, P < .01, respectively).
A minimum of 8 was scored on the FAQ subscale I. Forty-five percent of the subjects in the OI group scored a 10, 45% scored a 9, and 10% scored an 8 on the FAQ subscale I. Although subscales II and III of the FAQ are not validated, 69% of the subjects in the OI group reported limitations in walking, with the most frequent response being decreased endurance followed by weakness and pain. Those in the OI group also reported inability to ride a 2-wheel bicycle without training wheels (45%) and were unable to perform tasks such as jumping rope (40%), hopping on 1 foot (30%), and ice skating (65%) (Table 4).
There was a significant positive correlation between ankle plantar flexion as well as dorsiflexion isometric strength and the FAQ subscales I and III (Table 5). Specifically, plantar flexion strength significantly correlated with hopping on 1 foot, riding a 2-wheel bicycle without training wheels, and climbing stairs without using a handrail. Dorsiflexion strength also significantly correlated with running well around a corner, hopping on 1 foot, climbing stairs without a rail, and riding a 2-wheel bicycle without training wheels.
Seventeen subjects in the OI group reported a sedentary lifestyle, whereas 3 of the 20 subjects reported a high level of physical activity and sports involvement. One teen in the OI group played competitive soccer involving daily practices, another teen was a ballerina dancer, and 1 teen played recreational basketball.
At the time of testing, 17 of the 20 subjects in the OI group reported no pain during the physical examination. One child reported minimal thigh pain, another reported lower leg pain due to a rod protruding at the tibia, and a third child reported minimal back pain. All subjects in the control group reported no pain at the time of testing. Seventy-one percent of parents of subjects in the OI group reported that their son/daughter experienced pain in the past month. Six of the 20 subjects with OI reported pain levels to be between 1.5 and 6 when completing the FPS-R. The pain was identified as very mild to moderate in nature and did not necessarily limit the subject's activity level. All subjects who reported pain continued to participate in regular daily activities.
Children and adolescents with type I OI demonstrate weakness in their ankle plantar flexors compared with their age-matched peers who are developing typically. This is reflected in their reports on the PODCI and FAQ indicating difficulty in accomplishing higher-level gross motor skills that require adequate ankle plantar flexor strength. Improving ankle plantar flexor strength in children and adolescents with OI may allow them to more easily perform advanced skills such as running, jumping, hopping, negotiating stairs, and walking efficiently.
Children and adolescents with type I OI are generally functional in performing necessary daily activities of life; however, they may present with activity and strength limitations when evaluated more thoroughly. Many authors have noted the importance of upper- and lower-body strength in performing daily living skills for children with OI.22,32 Takken et al5 reported that subjects with type I OI had significantly reduced exercise tolerance and reduced muscle strength of the shoulder abductors, hip flexors, ankle dorsiflexors, and grip strength when compared with an age-matched control group. They concluded that exercise tolerance and muscle strength were significantly reduced in children with OI.5 Montpetit et al18 also found that children with varied types of OI had a weaker grip force than their age-matched peers, which was an indicator of severity of the disease. Our findings support these previous studies, specifically looking at ankle plantar flexor strength.
Graf et al33 reported that children with type I OI demonstrated gait deviations at the ankle that could be attributed to a combination of muscle weakness, ligamentous laxity, and avoidance of excessive forces on a fragile skeletal system. Specifically, they demonstrated delayed toe off with a reduced ankle power generation during push off, as well as decreased ankle plantar flexion range of motion, which may be the child's or teen's way of avoiding excessive forces on the fragile bones. In addition, Graf et al reported greater ankle power absorption in children with type I OI compared with the control group, which again may be due to ankle plantar flexor muscle weakness.31 Ankle plantar flexors play an important role in walking as greater than 40% of power production for walking is generated by the plantar flexors at push off.34
The Biodex strength test and heel-rise test confirmed ankle plantar flexor weakness in children and adolescents with type I OI. The pros of doing the heel-rise test include ease of administration, objective measurement values, and the ability to administer the test in most settings. The cons of the heel-rise test include subjective ratings of the distance the heel must rise from the floor, possible knee flexion to compensate for weak plantar flexors, decreased sensitivity to very minor changes in strength, and for very young children, difficulty in following verbal instructions. Many pros exist for the Biodex System 3, including standardized setup for each individual, exact/accurate numerical values assigned to strength measurements to the nearest tenth of a Newton meter (N m), controlled resistance, easily adjustable to fit a wide size range of individuals, and visual feedback. The negative aspects of this device include the large space it occupies in a clinic or rehabilitation gymnasium, decreased portability of the device, weight, and its high cost.
In this age range, children and adolescents who are developing typically exhibit a wide variability in strength capabilities. Children and adolescents in our control group demonstrated a wide range of strength values for isometric ankle plantar flexion strength measured on the Biodex, even when adjusted for age. Plantar flexion isometric strength testing strongly correlated with activity performance on the FAQ in the OI group, suggesting that targeted strengthening of the gastroc soleus complex may improve overall function.
Children and adolescents with type I OI are highly functional but exhibit limitations compared with their peers of similar age in such areas as sports, walking up and down stairs without a railing, riding a 2-wheel bicycle, hopping, and jumping. On the basis of our findings, children and adolescents with type I OI would benefit from baseline physical therapy services to monitor their changing needs and to provide necessary care as fractures occur and heal. An initial baseline physical therapy evaluation would be able to detect early signs of strength deficits from which strengthening exercises and home program instructions could be developed. As these children and adolescents go through periods of fracture and immobility, weakness develops and overall mobility decreases. Specifically, following a lower extremity fracture, physical therapy is warranted to improve muscle strength secondary to strength losses during the immobilization period. Once a fracture has healed and weight bearing is allowed, strengthening, walking, and exercise will help children and adolescents with OI return to their prior level of function.17
A physical therapy program for children and adolescents with OI who are ambulatory could encompass a progressive strengthening program with the addition of stair climbing, walking uphill on a treadmill or land, Thera-band (Akron, Ohio) exercises, elliptical training, aquatic exercises, stationary cycling, and Biodex training. Ongoing exercise and periodic consultative physical therapy can help develop and maintain strong muscles and bones in individuals with type I OI.32 Encouraging involvement in extracurricular, recreational, low-impact, noncontact activities may also be beneficial.35
To date, few published studies have reported how strengthening programs affect functional mobility and skill level in children and adolescents with mild OI. A recent study by Van Brussel et al reported a 3-month standardized functional fitness training program.7 They noted that aerobic and strengthening exercises for 25 to 35 minutes at a time, with a 5-minute warm-up and cool down, can significantly increase aerobic performance and muscle strength while decreasing fatigue in children with types I and IV OI.7 Gerber et al35,36 suggest hip extensor, abductor, and spinal musculature strengthening along with the use of a swimming pool and bracing, if indicated, to ensure continued upright and ambulatory activity. Further work in the area of strengthening various muscle groups and how strength relates to functional skills and ambulation is warranted.
In this study, the heel-rise test significantly correlated to peak plantar flexion torque tested on the Biodex System 3 Dynamometer. Although Wiggin et al37 reported quadriceps and hamstring isokinetic strength as tested on the Biodex System 3 Dynamometer for children aged 6 to 13 years who were developing typically, there have not been any studies using the Biodex System 3 Dynamometer to establish normative data for ankle plantar flexors. Similarly, there have not been any normative data published on isometric strength of children and adolescents with OI.
Zack et al6 reported on 79 children with OI who rated their pain using the visual analogue scale, with the majority of children reporting nonfracture pain at least 1 day a week with no identifiable etiology. Similar results were found in the present study. Interestingly, all children and adolescents who reported pain continued to participate in regular daily activities. Improved pain management may help alleviate symptoms and increase the level of functional mobility/physical activity that a child with OI can tolerate, and therefore, lead to improved strength and overall quality of life.
Limitations of this study include our small sample size. Strength assessment of additional muscle groups using the Biodex would have also been beneficial. The Gross Motor Function Measure—66 part E is another outcome tool that looks at higher-level functional skills, such as jumping, climbing stairs, hopping, kicking, and running,38 and could have been used to assess the gross motor skills of our subjects. Ruck-Gibis et al39 established the Gross Motor Function Measure as a reliable assessment tool for children with OI. Finally, it would be valuable to continue with this study and have subjects in the OI group perform a specific ankle plantar flexor strengthening program to see whether this alters their strength, functional abilities, and gait characteristics.
Children and adolescents with type I OI who appear to be highly functional may present with underlying decreased ankle plantar flexor strength and significant limitations in sports and physical function and pain/comfort. Their level of impairment is highly variable and changes dramatically because of fracture occurrence. Our study found the FAQ, FPS-R, and PODCI, along with muscle strength assessment, all to be useful assessment instruments for the evaluation of children/adolescents with type I OI. Individual limitations identified by these tools will guide clinicians in developing intervention strategies for these children. Children with OI have functional skills that can range from very limited to highly functional depending on the severity of their disease. Weak plantar flexor strength measured by the heel-rise test and the Biodex may require specific strengthening exercises, such as progressive loading of the ankle plantar flexors, which could in turn improve physical function. Further investigation of generalized upper/lower extremity conditioning through low–impact physical activities would also be beneficial to maximize functional abilities and quality of life. Future work in identifying fracture risk may also be a useful adjunct to current approaches for enhancing strength and functional abilities in children and adolescents with OI.
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activities of daily living; adolescent; child; muscle strength; osteogenesis imperfecta
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