External fixation has been commonly used for deformity correction, limb lengthening, treatment of open fracture, and reconstruction of bone defects. The advantages of this method include gradual correction and lengthening, adjustment of precision alignment, and comparatively rigid immobilization without being invasive to the correction segment and surrounding soft tissue. Long-term treatment is not uncommon and has the risk of complications such as pin-tract and deep infection, joint contractures, immobilization osteoporosis, and psychological problems.1 Hence, the reliable evaluation of callus maturation and the decision to remove a fixator are important topics in orthopedic surgery. However, the timing for removal of a fixator has been guided by radiographic examinations and clinical findings. Problems such as callus fracture and axis deviation can occur after premature removal of a fixator.1–3
Measurement of impedance is widely used in many industries when evaluating the physical properties of products. The most familiar devices using measurement of bioimpedance are body composition and cardiac output monitors. Various techniques to measure electrical impedance and conductivity in hard tissue are being developed for clinical application. Guimerà et al4 are currently developing a method and a device for measuring bio-impedance to assess bone mineral density, bone fracture healing, and dental caries. In spinal surgery, Bolger et al5 used electrical conductivity to avoid iatrogenic pedicle screw misplacement. Bonifasi-Lista and Cherkaev6 described the use of electrical impedance spectroscopy to evaluate osteoporosis. Dai et al7 devised a method using electrical impedance during drilling of bone tissue to monitor the position of the drill tip to avoid drilling past the contralateral cortex and causing soft tissue injury. Hirashima et al8 measured overall impedance in patients with a distal end fracture of the radius, reporting that impedance values increased concomitantly with bone union.
The current authors measured bioelectrical impedance in patients undergoing deformity correction or callus distraction using an external fixator. An alternating current device9 and impedance calculator (MES Co, Ltd, Tokyo, Japan), both small pieces of equipment, are used. Impedance values can be measured in a few minutes. With this method, steel pins inserted for an external fixator can be used as electrodes to measure bioelectrical impedance in bone during callus maturation for easy, noninvasive, and continuous monitoring.
In this study, the temporal changes in impedance values were analyzed over time during the callus maturation process. Because age, correction site, and treatment method differ for individual patients, resistance rates of sufficient maturity callus were calculated when the external fixator was removed. The resistance rates were also compared by age, correction site, and treatment method.
Materials and Methods
This study was approved by the ethical review board of the authors' institution. Thirty-one patients (41 limbs) who underwent osteotomy for deformity correction or callus distraction using an external fixator between 2004 and 2012 were included. The following cases were excluded because of plate conversion and complications around the steel pin site for measurements: lengthening and then plating for conversion to internal fixation10 in 5 limbs, breakage of the pin for measurement in 1 limb, severe infection around the pin for measurement in 6 limbs, and metatarsal distraction in 2 limbs. Thus, 23 patients (27 limbs) were included in the analysis.
Mean patient age at the time of surgery was 17.2 years (range, 4–58 years). The correction sites involved the femur in 12 patients, the tibia in 13 patients, and the ulna in 2 patients. The following external fixators were used: the Dynafix and the EBI (EBI, Parsippany, New Jersey) in 9 limbs, the Ilizarov (insulated around the pins for measurement) in 9 limbs, the Orthofix (Orthofix, Verona, Italy) in 8 limbs, and the Taylor Spatial Frame (Smith & Nephew, Memphis, Tennessee) in 1 limb.
Measurement of Overall Impedance
Impedance values fluctuate during deformity correction and callus distraction because the distance between the measurement pins changes. Therefore, overall impedance measurements were started after completion of correction and distraction using the most proximally and distally inserted pins at the correction sites as electrodes. The overall impedance (Z [kΩ]) between the pins was measured using the alternating current device and impedance calculator. Alternating current was applied using the device with a constant current output of 30±6 µA and loading resistance of 0 to 60 kΩ. The frequency was set to 2±0.4 Hz to limit the reactance element of alternating current to a negligible range during measurement.
Impedance values were measured at outpatient clinics during callus maturation from after correction or distraction to removal of the fixator. Temporal changes were measured, maximum and final values were compared with initial values, and rates of change based on the initial values were calculated. The mean duration of impedance measurement from after completion of correction or distraction until removal of the fixator was 18.6 weeks (range, 10–64 weeks).
Resistance Rate Between Pins
The bone and distraction callus from the proximal pin region to the distal pin region was assumed to resemble a cylindrical conductor, and the resistance rate (ρ [Ωm]) of each group was calculated as follows. The transverse diameter (a-values) and anteroposterior diameter (b-values) of the proximal pin region, the middle of the callus, and the distal pin region were designated as a1, a2, and a3 and b1, b2, and b3, respectively, and measured radiographically. Their cross-sectional areas (Amean [m2]) were calculated using the equation in Figure 1.
Photographs showing measurement of electrical resistance rates between the proximal and the distal pin regions. The resistance rate was calculated by measuring transverse diameter and anteroposterior diameter at the proximal pin region, maturation callus site, and distal pin region. Bone tissue was assumed to be in the shape of an oval column based on averaging of these values (A). Diagram illustrating measurement of mean cross-sectional area (Amean) and the resistance rate (ρ) (B).
The length between the proximal pin region and the distal pin region was designated L [m]. The resistance rate was calculated with the formula in Figure 1.11
The calculated resistance rates were classified by age, correction site, and treatment method. Age was younger than 15 years (14 limbs) and 15 years or older (13 limbs), site was the femur (12 limbs) and the tibia (13 limbs), and treatment method was noncontact (19 limbs: no cortical contact between bone fragments during correction or distraction such as rotation correction) and contact (8 limbs: cortical contact between bone fragments as with hemicallotasis or acute deformity correction).
Temporal changes in overall impedance were measured, and maximum values and final values at sufficient callus maturation were compared with initial values. Because the duration of the measurement period varied for each patient, each period was divided into 10 equal intervals of 0.1, and the rates of increase in each case were plotted to evaluate temporal changes in overall impedance. Resistance rates were compared by age, correction site, and treatment method. Multiple regression analysis was performed with resistance rate as the dependent variable and age, correction site, and treatment method as the independent variables.
Testing between groups was performed using the Welch's t test. Testing among multiple groups was performed using single-factor analysis of variance and the Kruskal–Wallis test. Multiple regression analysis was performed using SPSS version 22 software (IBM SPSS Statistics, Chicago, Illinois).
Temporal changes in overall impedance were measured in 27 limbs. The mean maximum and final impedance values were 1.21±0.19 times and 1.15±0.20 times higher, respectively, than the initial values (P<.01 and P<.01, respectively) (Figure 2).
Graph showing temporal changes in overall impedance. These changes and rates of increase vary among patients. The mean maximum and final impedance values are 1.21 times and 1.15 times higher, respectively, than the baseline values; these differences are significant.
The mean rate of change based on the initial values showed a gradual increase from after completion of correction or distraction to callus maturation, increasing significantly compared with baseline for 70% or greater of the callus maturation period (Figure 3).
Graph showing the mean rate of change based on the values at completion of correction or distraction until callus maturation. The rate of change of the impedance values is significantly increased compared with baseline for 70% or greater of the callus maturation period. Abbreviation: ANOVA, analysis of variance.
Comparison of the resistance rates (ρ) showed a significant difference between age younger than 15 years (3.8±1.3 Ωm) and age 15 years or older (6.4±2.9 Ωm; P<.01; Figure 4A). Resistance rates (ρ) also differed significantly by correction site (femur 3.7±1.4 Ωm vs tibia 6.4±2.8 Ωm; P<.01; Figure 4B) and by treatment method (noncontact 4.2±2.2 Ωm vs contact 7.1±2.1 Ωm; P<.01; Figure 4C).
Comparison of resistance rates showing significant differences between age younger than 15 years vs 15 years or older (A), correction sites (femur vs tibia) (B), and treatment methods (noncontact vs contact) (C). aP<.01 by Welch's t test.
Multiple regression analysis was performed with resistance rate as the dependent variable. The most reliable formula in the stepwise multiple regression analysis was calculated as:
This study investigated measurements of bioelectrical impedance for monitoring of callus maturation after osteotomy for deformity correction or callus distraction. Resistance rates were also calculated by patient age, correction site, and treatment method. There was a gradual temporal increase in mean overall impedance, and maximum and final impedance values were significantly increased from baseline. The resistance rates also differed significantly by age, correction site, and treatment method. Multiple regression analysis showed that age and treatment method were useful predictors for the resistance rate.
Regarding measurement of impedance in bone, Kawamoto et al9 investigated the enhancement of distraction callus maturation and measured the impedance of excised bone in rabbits. They reported significantly increased impedance values in the accelerated callus maturation group compared with the control group. The current authors also assessed fracture and distraction callus in rabbits by monitoring the electrical impedance of bone, finding that the temporal increases in overall impedance reflect callus maturation.11,12 However, measurement of impedance in patients treated with an external fixator during the callus maturation process after correction or distraction has not been previously reported.
Impedance measurements are evaluated in tissues composed of conductive electrolytes in relatively nonconductive skin tissue. During monitoring of callus maturation, impedance increases due to soft and hard callus formation and narrowing of the transverse diameter with bone medullarization and corticalization. The current study found that overall impedance tended to increase, in a manner similar to that seen in previous animal studies and a clinical study of distal radius fractures.8,11,12 However, unlike in previous research, age, correction site, and treatment methods differed among patients, thus leading to a wide variation in impedance changes and rates of increase in individual cases. The current authors thought that callus maturation could be quantified using impedance measurements. However, the data were still insufficient for clinical application to determine when an external fixator could be safely removed.
Therefore, to classify differences in each patient, characteristic resistance rates in each substance were considered. Resistance rates are largely determined based on microstructure and type of electrical conductive material.13 Weast and Astle14 measured resistance rates in representative tissues, reporting values of 0.6 Ωm in blood, 2.5 Ωm in muscle, 30,000 Ωm in dry bone, and 30 Ωm in cortical bone moistened with physiological saline. In the current study, resistance rates were calculated after sufficient callus maturation, and it was found that resistance rates differed significantly by age, correction site, and treatment method.
Resistance rates were higher in patients 15 years or older. Black and Mattson15 and Kosterich et al16 reported that, in cortical bone, current is transmitted through the Haversian and Volkmann canals occupying approximately 5% of internal void volume. They suggested that there is an increase in conductivity when laminar structure is repaired. Children have rich blood flow and high water content; their bone is still immature, resulting in lower resistance rates.
Regarding correction site, the cortex/medulla area ratios between the femur and the tibia are different. Weast and Astle14 also reported that increased intramedullary blood volume is associated with a decrease in the intramedullary resistance rate. Therefore, in the tibia, which has a higher percentage of cortical bone and a smaller cross-sectional diameter, the resistance rate is higher.
Regarding treatment method, the non-contact group had more callus formation than the contact group. Because the water content in the microstructure was higher, the conductivity was greater and the resistance rate was lower.
Limitations of the current study included the small number of cases and that the resistance rate was evaluated in all of the tissue, including the soft tissue between the inserted steel pins. This is in contrast to animal studies, in which soft tissue was removed and the resistance rate of only bone was measured.11,12 However, clinically, both bone healing and soft tissue healing are necessary for bone repair and callus maturation. Thus, the resistance rates found in the current study, which differed by age, correction site, and treatment method, may provide important data for future bioelectrical impedance analyses of tissues of extremities.
This study showed resistance rates that differed by age, correction site, and treatment method. Age and treatment method were also important predictors of the resistance rate. Using these data, the length between the proximal pin region and the distal pin region, and the transverse diameter (a-values) and the anteroposterior diameter (b-values) of the callus after completion of correction or distraction, overall impedance at the time of sufficient callus maturation will be assumed, according to calculation with the formula: (overall impedance)=(resistance rate)× L/Amean. Therefore, the current findings may serve as a useful index to determine when an external fixator should be removed. Further research regarding impedance multiplier application is needed for practical use of this method.
This study measured bioelectrical impedance to monitor callus maturation after osteotomy for deformity correction or callus distraction. Resistance rates were also calculated according to patient age, correction site, and treatment method. There was a gradual temporal increase in overall impedance during callus maturation. Mean maximum and final impedance values were 1.21 times and 1.15 times higher, respectively, than initial values, with both of these increases being significant. Resistance rates differed significantly by age, correction site, and treatment method. Age and treatment method were important predictors of resistance rates. These resistance rates, which assume overall impedance during callus maturation, may serve as a useful index to determine when an external fixator should be removed.
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