Monitoring of Distraction in Hypertrophic Nonunions

The individual steps in gradual distraction during the treatment of hypertrophic nonunions have been followed up at our department with radiographic, echographic, extensimetric, and histological studies. Therefore, qualitative morphological information provided by x-rays and ultrasound scans (and whenever possible by histological studies) were complemented by quantitative functional information provided by extensimetric data.

Some Authors have reported the use of additional methods of monitoring new bone formation during distraction. Mazess [32], Eyres et al. [33], and Reiter et al. [34] described a quantitative assessment of bone mineralization during the distraction procedure using dual photon or dual energy x-ray absorption, based on the measurement of the bone mineral density in the newly formed bone and in the adjacent bone. These studies provided a precise assessment of the mineralization, which is closely related to the stiffness, torsion, and stability of bone.

Tjernstrom et al. [35] and Iacobellis et al. [36] examined some anatomical characteristics and structural changes in the newly formed bone segments by means of CT and MRI evaluation. In comparison with the contralateral segment, CT showed variations in the dimensions and density of the cortical bone and the medullary canal [36].

These techniques may help to more accurately manage the distraction phases and reduce complications, but they are still quite difficult to use in routine clinical practice.

X-Ray Investigations

Evaluation by traditional radiographic methods shows the first signs of ossification as a slight, poorly defined, uniform opacity at the distraction site, crossed by longitudinal striations, 1 month after beginning the treatment. The opacity becomes darker between the first and second month while the longitudinal striations become wider and lean to fuse and the regenerating bone takes on the shape of an hourglass.

Radiographic investigations give only little information in the first stages (the first 4 weeks) but are nevertheless crucial in order to monitor the morphology of the bone during the lengthening period and to confirm the right connection between the bone extremities.

After 3 months from the beginning of treatment, a thin shell of cortical bone appears, becoming gradually thicker. The external fixator can be removed on average after 5 months (Figs. 5-12).

The device can be removed once the new bone formed in the distraction gap demonstrates bridging neocorticalization on at least three sides on orthogonal radiographs [15,20,37,38].

Ultrasound Scan

The need to reduce the high dose of radiation while at the same time obtaining clear information about the earliest phases of development of the bone regeneration makes ultrasound evaluation especially useful [20, 38-44]. During the first phases of bone distraction, a hypoechogenic band is found between the bone extremities. After nearly 3 weeks the process of bone regeneration can be seen as an echogenic signal. Later (nearly 2 months afterwards) transmission of the ultrasound waves is reduced by this echogenic material; after 3 months the regenerating bone appears as an echogenic stripe between the two extremities of the cortical bone. In the last part of the treatment period (4 months from the beginning, on average) the cortex appears uninterrupted (Figs. 13-15).

Once treatment is completed, ultrasound is less relevant due to the fact that the wave given from the probe is highly reflected from the mineralized bone.

The ultrasound evaluation is important also to identify any abnormality in regenerating bone. Three types of regenerating bone formation can be observed by ultrasound [44] (Figs. 16,17).

Fig. 5a, b. X-rays of a hypertro-phic nonunion of the right tibia in a 68-year-old woman
Fig. 6a, b. Same case as in Fig. 5. Stabilization with an Ilizarov device and gradual distraction of the nonunion site
Fig. 7a, b. Same case as in Fig. 5. Healing of the nonunion after 2 months and 20 days
Fig. 8a, b. X-rays of a hypertrophic nonunion with shortening after open reduction and internal fixation of a fracture of the distal third of the left humerus
Fig.9. Same case as in Fig. 8. After the removal of plate and screws an Ilizarov circular external fixa-tor was applied and then gradual distraction was started.
Fig. 10. Same case as in Fig. 8. Sonographic control at the same time of the radiographic control shown in Fig. 7
Fig. 11a, b. Same case as in Fig. 8. a X-ray 2 weeks after the beginning of distraction. b X-ray at the end of the distraction phase
Fig. 12. Same case as in Fig. 9. Healing of the nonunion after 3 months
Fig. 13. Sonographic features of the initial phases of bone distraction: an hypoechogenic band between the bone extremities is seen
Fig. 14a, b. a Echogenic material is observed 3 weeks after the beginning of the distraction. b After 2 months, transmission of ultrasounds is reduced
Fig. 15. After 3 months an echo-genic stripe between the bone ends is seen
Fig.16. Sonographic features of normal bone regeneration
Fig. 17a, b. Sonographic features of hypotrophic (cystic) distraction osteo-genesis (a), and of hypertrophic bone regeneration (b)

In the first phase of distraction normal regeneration shows an abundant presence of fibrous tissue, followed by a normal beginning of mineralization after the first 30-40 days. In hypotrophic (cystic) regeneration, a narrowing of the regenerating bone and a lacunar image in the regenerated bone is observed. Then the distraction must be stopped or slowed to obtain a gradual disappearing of the cyst and to avoid an insufficient or delayed consolidation.

In hypertrophic regeneration an abnormal abundance of fibrous tissue is observed, and a sonographic gap that is smaller than the radiographic gap is seen between the bone ends. In these cases the distraction speed must be increased for 7-10 days in order to prevent an early consolidation.


Using extensimetry, the mechanical properties of the regenerating bone can be quantified by evaluating the deformation of the system bone-fixator at different stages of bone consolidation [20,45,46] (Fig. 18).

During fracture healing, an increase in mechanical resistance is observed at the same time as consolidation of the regenerating bone. This increased resistance is related to the progression of regenerating bone through different mechanical phases that correspond to specific biologic phases. They can be detected with tests such as flexo-extension, bending, and walking (periodically performed every 20 days):

1. Initial phase (different deformation according to the different kind of assembly;

2. Phase of maximal deformability, which corresponds to a maximum plasticity of the regenerating bone;

3. Phase of reducing the deformation, related to progressive calcification;

4. Phase of mechanical stability, which shows minimal readings of deformation and correspond to corticalization of the regenerating bone;

5. Final phase of secondary deformability (due to the process of bone remodeling).

Morphologic Study

In eight cases, material for morphological examination of the nonunion site could be obtained at different time intervals from the beginning of distraction treatment and while associated lesions requiring a surgical approach were being treated. Biopsy material was in part fixed in 4% phosphate-buffered formaldehyde, pH 7.2, at room temperature and dehydrated in graded series of ethanol. After embedding in paraffin, blocks were serially sectioned at 7 ^m and the sections stained with hematoxylin-eosin. Some of the specimens were fixed in 2.5% glutaraldehyde, pH 7.3, and postfixed in OsO4. The tissues were dehydrated in graded series of ethanol and embedded in Epon 812 resin. Semithin sections were then stained with Rosenqvist silver stain.

In the very first phases, nonunion tissue is seen histologically as hypovas-cular fibrous or fibrocartilaginous tissue with very few capillaries and nearly always empty. The aspect of the nonunion tissue contrasts with the hypervas-cular bone ends on either side.

Fig. 18 a,b. Extensimetric device applied to an Ilizarov apparatus, in order to evaluate the mechanical properties of the regenerating bone

Ten days after the beginning of distraction, there is a high proliferation of capillaries that form a vascular net and they are no longer empty but rather are filled by red blood cells. After 20 days there are fascicles of fibroblasts parallel to the lines of distractional stress.

In more advanced phases there is a gradual differentiation of osteoblasts that start to form osteoid tissue and then deposits of calcium salt are observed between the collagenic fibers and inside the organic matrix of the osteoid. Two months and half after after distracton is applied, the new bone trabeculae can be readily identified (Figs. 19-27).

Fig. 19. Micrograph of an hypertrophic nonunion. The nonunion tissue (on the left side) appears as a fibrous hypovascular tissue (Hematoxylin and Eosin, original magnification: x 100)
Fig.20. In the fibrous tissue of the nonunion very few capillaries are seen (Hematoxylin and Eosin, original magnification: x 250)
Fig. 21. Proliferation of capillaries 10 days after the beginning of distraction (Hematoxylin and Eosin, original magnification: x 250)
Fig.22. At higher magnification, capillaries appear filled by red blood cells (Hematoxylin and Eosin, original magnification: x 400)
Fig. 23. Twenty days after the beginning of distraction, fascicles of fi-broblasts parallel to to the lines of distraction-al stress are seen (He-matoxylin and Eosin, original magnification: x 250)
Fig. 24. Same field as in Fig. 16 at higher magnification (Hematoxylin and Eosin, original magnification: x 400)
Fig.25. Differentiation of osteoblasts (with deposition of osteoid substance and calcium salts) and gradual transformation into osteocytes. (Rosenqvist silver stain, original magnification: x 1250)
Fig.26. Osteoid substance with osteocytic lacunae (semi-thin section, Rosenqvist silver stain, original magnification: x 1250)

Fig. 27. New bone tra-beculae are clearly seen 2 months after the beginning of distraction (Hematoxylin and Eosin, original magnification: x 100)

This morphologic study, performed for the first time on human specimens (from eight patients), has clarified some obscure and controversial points regarding the evolution of the nonunion site under the action of tension forces. In particular it has shown the intensive stimulus to neoangiogenesis (seen from the first days of the distraction treatment).

The study has also shown the absence of a cartilaginous stage between the initial tissue and the new bone, and so the process can be considered as a membranous ossification and not an enchondral ossification. Moreover, the evaluation of the histological patterns confirmed that the process of osteoge-nesis does not proceed in a sequential manner but evolves in stages that overlap, as underlined by Tajana et al. [47],so that it is possible to observe different stages in one specimen.

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