compmarative study of the effect of ultrasound and electrostimulation on bone healing in rats

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Ovid: Zorlu: Am J Phys Med Rehabil, Volume 77(5).September/October 1998.427-432

Williams & Wilkins 1998. All Rights Reserved. Volume 77(5), September/October 1998, pp 427-432COMPARATIVE STUDY OF THE EFFECT OF ULTRASOUND AND

ELECTROSTIMULATION ON BONE HEALING IN RATS1[CME Article]

Zorlu, mran MD; Tercan, Mustafa MD2; zyazgan, Irfan MD; Taskan, Isik MD; Kardas, Yildiz MD; Balkar, Faruk MD; ztrk, Figen MD

1From the Department of Physical Therapy and Rehabilitation, The State Hospital of Antalya, Antalya, Turkey (Z); the Department of Plastic and Reconstructive Surgery, Medical Faculty of Inonu University, Malatya, Turkey (MT); the Departments of Plastic and Reconstructive Surgery (I), Physical Therapy and Rehabilitation (YK), Orthopedics and Traumatology (FB), and Pathology (F), the Medical Faculty of Erciyes University, Kayseri, Turkey; the Physical Therapy and Rehabilitation Center, Istanbul, Turkey.2All correspondence and requests for reprints should be addressed to: Inonu Universitesi, TIP Fakultesi, Plastik ve Rekonstruktif, Cerrahi ABD, Malatya 44069, Turkey.1998 Series Number 15

ABSTRACT

This study was performed to compare the effects of direct current with ultrasound on fracture healing. Thirty-two rats were subjected to the experiment. Each rat's right legs were used as the experimental sample, and their left legs were used as the control. Four groups were formed, each consisting of 16 ultrasound, 16 electrostimulation, 16 ultrasound control, and 16 electrostimulation control animals. Fibular osteotome was applied to the rats under anesthesia. In the electrostimulation and electrostimulation control groups, a stainless steel cathode electrode was installed in the fractured side. In the electrostimulation group, 10 A of direct current for 30 min, using a semi-invasive method, was given one day after fracture, for 15 days. On the control side, the aforementioned protocol was followed but sham treated. The ultrasound group was treated with 0.1 W/cm2 ultrasound for 2 min every second day for 6 days after fracture (4 times). Rats were killed on the 7th and 14th days to investigate the macroscopic, radiologic, and histopathologic parameters of fracture healing. There was a difference (P < 0.05) between the electrostimulation and the electrostimulation control groups on the 7th day. There was a difference (P < 0.05) between the ultrasound and ultrasound control groups on the 14th day. After statistical evaluation of the experimental results, it was found that in both the ultrasound and the electrostimulation groups, the fracture healing had been accelerated more so than in the control groups. There was no observed statistical difference between ultrasound and electrostimulation effects.

Objectives: Upon completion of this article, the reader should be able to (1) differentiate the effect of ultrasound and electrostimulation on bone union; (2) determine the

confidentiality of the biomechanical tests; (3) assess the value of the growth promotor factor in the bone. Level: Advanced

The Association of Academic Physiatrists is accredited by the Accreditation Council for Continuing Medical Education to sponsor continuing medical education for physicians.

The Association of Academic Physiatrists designates this continuing medical education activity for a maximum of one credit hour in Category 1 of the Physician's Recognition

Award of the American Medical Association. Each physician should claim only those hours of credit that he/she actually spent in the educational activity.

*Disclosure statements have been obtained regarding the authors' relationships with financial supporters of this activity. There is no apparent conflict of interest related to the

context of participation of the authors of this article.

Bone healing takes a long time, causes complications, and eventually leads to a loss of manpower and raised costs. Various methods have been used to accelerate bone healing.

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Electrical stimulation (ES) and ultrasound (US) are only two of the methods tried.

The accelerating effect of ES on nonunion and delayed union treatment has been reported. Although there has been some controversy about fresh bone fracture treated with

direct current,1 bone healing can be accelerated when treated with suitable methods.2-11

Studies have shown the beneficial effect of US on bone healing, although only a few studies have been performed in this respect.12-16 It has been suggested that applying ES

30 min daily for 2 to 3 wk and US 2 min daily every other day is sufficient to accelerate bone healing.2, 5, 6, 8, 10, 11, 14, 15 There is no evidence of deleterious effects from these

treatment modalities when they are used properly. The various effects of both ES and US on bone healing have been reported, but no comparative study has been undertaken.

We performed this study to evaluate and to compare the effect of US with ES on bone healing.

MATERIAL AND METHODS

Thirty-two Sprague-Dawley rats weighing 230 to 300 g were used. All rats were individually housed and fed standard rat chow ad libitum throughout the experiment. Anesthesia

was achieved by ketamine hydrochloride (6 mg/kg) and 0.1 mg of atropine intraperitoneally. After preparation of the hindlimb, flexion position was given. A 1-cm linear incision

was made on the lateral aspect of the limb. The fibular bone was exposed after passing the intermuscularly septum. A small pair of scissors was used to make an experimental

fracture in the middle third of the fibula.

All rats were divided into either the electrostimulation group or the ultrasound group. The right hindlimbs of the rats were used as the experimental sides, and the left hindlimbs

were used as the control sides. Eventually, all 16 hindlimbs were used in the electrostimulation groups, sham electrostimulation group, ultrasound group, and sham ultrasound

group. All 64 fibular bones were used in the study.

Electrostimulation Group

After the bone was fractured, stainless steel was wrapped around the fracture site in a semi-invasive technique, according to the method of Paterson et al.17 One end of the

steel was placed outside the skin to enable contact with the electrode of the electrostimulation device. After bleeding was controlled, the incision was closed with 5-0 silk

sutures. No splints were used throughout the experiment. The rats were allowed to move freely in their cages. Rats were stabilized on a board 24 hr after their operations. A

cathode electrode electrostimulation device (Dynaproge 527; Enraf, Nonius, The Netherlands) was used to make contact with the exposed end of the steel. The anode electrode

was placed on the fracture site proximally by using pads moistened with a saline solution. Direct current was applied by means of negative polarity with 10 A 30 min daily for

15 days.

Sham Electrostimulation Group

The same procedure was undertaken as in Group 1, except no current was applied.

Ultrasound Grouphttp://gateway.ut.ovid.com/gw1/ovidweb.cgi (2 of 11)04.02.2007 00:22:00


The same fracture pattern was used. A pulsed US (0.1 W/cm2 intensity) was applied by the moving applicator technique for 2 min on alternate days, as reported by Reuter et

al.14

Sham Ultrasound Group

The procedure was the same as that performed in Group 3 rats but with the device off. All wounds were cleaned using a povidone-iodine solution before and after the

procedures. One-half of the rats in each group were killed on the 7th and 14th days. After releasing their muscular attachments, both fibula and tibia bones were removed

together. Double-blind evaluations were performed.

EvaluationsMacroscopy

Fracture ends were evaluated in relation to each other and scored as follows: Score 1 = mobile, easy to manipulate; Score 2 = elastic, angulation by manipulation; Score 3 =

solid, stable fracture site. Also, the fracture site was carefully observed to detect bridging. After macroscopic evaluation, the tibiofibulare joint was detached and the fibular bone

was placed in 10% buffered formalin.

Radiology

X-rays were taken on the 7th and 14th days after the operation. Films magnified 3 were evaluated by the same radiologist. The evaluation was made according to callus

formation and scored as follows: periosteal callus-Score 1 = beginning stage of periosteal callus, Score 2 = mature periosteal callus, and Score 3 = finishing stage of periosteal

callus; endosteal callus: Score 1 = beginning stage of endosteal callus, Score 2 = mature callus approximating the fractured ends, and Score 3 = completion of bone union.

The union criterion was accepted as a score of 6 (3 + 3). Bridging was accepted as a more advanced level of callus formation when callus formation existed; therefore, one

point was added. In addition, the arrangement of the callus was evaluated.

Histopathology

Tissues were stained with hematoxylin and eosin. Evaluation of callus formation was made using two different methods: (1) histologic scoring 18 (Table 1); (2) callus tissue

components were measured as percentile by the lane-sampling method.



TABLE 1 Histologic scoring

Statistical Analysis

Statistical analysis was made using the Mann-Whitney U test.

RESULTS

One rat in the ES group had hyperemia and edema on the 4th day. Cefradine, 60 mg/kg daily, was given as antibiotic therapy. The hyperemia and edema disappeared within 2

days. This rat was subjected to the same procedure as the other rats.

There were no differences between the US and ES groups both at the 7th and 14th days in the fracture ends (P > 0.05). Results are summarized in Table 2.



TABLE 2 Relation between fracture edges in groups

Radiologic evaluations were made to determine periosteal and endosteal callus formation at three stages on the 7th and 14th days. Careful observation for bridging formation

was undertaken. Periosteal callus formation was seen in all groups on the 7th day. There are differences between the ES and sham electrostimulation groups (P < 0.05) on the

7th day. Periosteal callus formation has advanced and begun to form an endosteal callus in the US and ES groups on the 14th day (P < 0.05). In addition, regular and well

arranged callus formation was detected in both the US and ES groups. Radiologic findings are summarized in the Table 3.

TABLE 3 Radiologic findings in groups

In the histologic evaluation, scoring was meaningful in the experimental groups both on the 7th and 14th days. When the groups were compared with regard to the composition

of callus tissue, classified cartilage tissue was dominant in the ES and US groups and fibrous tissue in the control groups. New bone formation was found as the beginning stage

in the experimental groups but not in the control groups. As fibrous and hyaline cartilage decreased in the US and ES groups, calcified cartilage tissue and new bone formation

increased compared with the control group by the 14th day. Because the increased level of the calcified cartilage in the ES and US groups indicates mineralization, increased



bony union indicates osteogenesis. Low-level fibrous tissue is an indication of transformation of fibrous tissue into the hyaline cartilage.

The fracture sites were evaluated and scored for bone union, spongiosa bone, and bone marrow. There were differences between the control and experimental groups on the

7th and 14th days (P < 0.05). Results are summarized in Table 4.

TABLE 4 Histologic scoring of callus in groups

The components of callus tissue were evaluated as percentiles according to the Lane-Sampling method. In the US and ES control groups, fibrous and hyalin cartilage

predominated in the callus tissue on the 7th day. There was no new bone union in these groups.

The beginning of new bone formation and a certain amount of calcified cartilage tissue were seen in both the ES and US groups on the 7th day (P < 0.05). The fibrous tissues

showed minimal calcified cartilage, and prominent new bone tissue was seen on the 14th day. There are differences between the experimental and control groups (P < 0.05;

Table 5).

TABLE 5 Average percentiles of callus components in groups

DISCUSSION

Treatment for both nonunion and delayed union of bone with direct current have been reported by various authors.19-25 ES has been used in the treatment of nonunion and http://gateway.ut.ovid.com/gw1/ovidweb.cgi (6 of 11)04.02.2007 00:22:00


delayed union of bone after showing a beneficial effect, and it became a routine procedure at some medical centers.2-8, 10, 11, 26-35

Biologic properties of fresh fracture, delayed union, and nonunion are quite different. Growth promoter factors, such as negative potentials, disappear in the nonunion of bone.

Fibrous and fibrocartilaginous tissues fill between the ends of the fractured bone. Controversially, hematoma occurs in the fresh bone fracture. In addition, perfusion decreases

in nonunion of bone. Cartilage and sclerotic bone reaction prevents vascular growth into the nonunion region. Applying weight to the fracture site has not proved to be

successful.36 The various factors mentioned above are thought to have differing effects on fresh bone fracture.

In this study, direct current using the semi-invasive technique was chosen as the method for ES. The osteogenetic effect of direct current has been shown by various authors.8,

20, 25 A semi-invasive technique was used to decrease the effect of surgery. We also used 10 A of direct current for 30 min daily. It has been stated to be the most effective

period of ES for the first 2 wk.16, 20 We also used ES for 2 wk. Stainless electrodes have been reported to be good conductors 7, 11, 20; therefore, we used that type of

electrode. Because of the small diameter of the fibula, we wrapped the electrode around the fibula as performed by Paterson et al.24

A total of 1.5 W/cm2 US, 5 min daily, for 15 days has been shown to have an accelerating effect on rabbit bone. In addition, the same dose is effective, even when administered

every third day.14 In contrast, callus formation was not increased by US.15

Reuter and colleagues 14 reported the effectiveness of US when applied with a 0.1 W/cm2 dose, 2 min every other day, for a total of four times.31, 37 This application caused an

increase in osteogenesis at the end of 2 wk.16, 32 Although the effect of US on mineralization and callus formation has a positive effect with the dose of 0.1 W/cm2 for 2 to 4

min, the dose of 1 W/cm2 is not effective on bone healing.13 We also used US in the dose of 0.1 W/cm,2 2 min every other day, for a total of four times. The first application of

US was on the 6th day of fracture. No other rat, except one, was given prophylactic antibiotic.

Biomechanical tests are confidential tests for the evaluation of fractures.36-38 Although the torsion test is used for the evaluation of bendable bones such as the fibula, we did

not use that test because of the weakness of the fibula and technical insufficiency. In lieu of this test, we evaluated the fractured ends to determine callus resistance.

By evaluating the ends of the fractures, there was a good relation in the ES group compared with the sham electrostimulation group. This finding is consistent with the

literature, which shows the effect of direct current 3, 8 and the increase of callus tissue before mineralization in the early stages of fracture healing.3, 4, 8 Although there is a

difference between the US and sham ultrasound groups, the results are not statistically significant. This result was concluded as being an ineffective measurement because of

minimal changes. Reuter and colleagues 14 did not find any differences between the groups at the 7th day. Both the US and the ES groups showed no differences when

compared with each other. Although there was no solid relation between the sham electrostimulation group and the sham ultrasound group on the 14th day, both solid and

elastic relations were determined between the US and ES groups.

It was seen that both ES and US treatment accelerate fracture healing. This finding also is consistent with the literature.2, 16, 20



We also detected increased vascularization and osteoblastic activity in the fractured ends after having used both ES and US. This was also supported by the relevant literature.3,

13, 16 By the 7th day, the beginning stages of periosteal callus were seen in all groups.

In the radiologic evaluation, the beginning stage of healing was observed in all four groups on the 7th day. These results are compatible with the literature, which indicates the

proliferation of osteoprogenitor cells on the 1st day, development of trabecula between the 3rd and 10th days, and observation of periosteal callus on the 5th day and endosteal

callus on the 11th day.39-43 Although there was no difference among the groups regarding the stage of callus, there was a difference between the ES and sham

electrostimulation groups when they were evaluated with the number of rats. These results are supported by the literature, which indicates an increase in callus formation when

direct current has been applied.3 In the radiologic evaluation, there was no difference between the US and sham ultrasound groups and the ES and sham electrostimulation

groups.

In our study, both the US and ES groups had completed callus formation earlier and much more so than the control groups did. These results are compatible with the study that

indicates US and direct current cause an increase in density, more callus formation, and mineralization,3, 13 and this effect is seen by the 14th day.2, 13, 16, 20 It is accepted that

electrical stimulation increases synthesis of DNA in osteoprogenitor cells and collagen production in fibroblast tissue medium and accelerates calcification of cartilage matrix.1, 9,

20 It has been shown that direct current increases the number of hydroxyl ions and pH and decreases the tissue oxygen level at the cathodic site.4, 9, 20

It has been reported that low oxygen pressure causes the bone formation and alkali pH to give rise to calcification in the tissue.2, 10 Also, direct current stimulates production of

cAMP in the cell by changing the cell surface potentials.4, 9, 20, 42

If direct current, which converts the periosteal cell into the osteoprogenitor cells, IS applied continuously, osteoprogenitor cells are converted into osteoblasts in the osteoid

tissue, but they are converted into fibrocyte after cutting off the current 24 hr later.3 A mineralization effect of direct current also has been reported in some articles.9, 20 In our

study, the increase in mineralization and osteogenesis in the ES group was attributed to the mechanism mentioned above.

It has been shown that US shortens inflammation phases and increases new vascular formation and activity of alkaline phosphatase and lysozyme by means of the piezoelectric

effect.13, 15 In our study, acceleration of osteogenesis in the US group was attributed to the piezoelectric effect.

As a result, cartilage formation from the fibrous tissue, mineralization, and new bone formation were seen in both the US and ES groups compared with the control groups.

These effects have been observed more so on the 14th day.

Although results are much better in the ES group than in the US group, there was no difference statistically. Better results were reported in the US group by Reuter and

colleagues.14, 15 Also, Reuter and colleagues reported that ES accelerates bone healing as much as 20 to 30 percent. In contrast, this effect was reported as 80 percent by

various other authors.9, 11 Application of the ES method in the study by Reuter et al. was ambiguous; therefore, a comparison could not be done.

In our study, both ES and US accelerates bone healing. US has the advantage of having 2-min applications daily, for a total of 8 min. US can be chosen because of its easy and http://gateway.ut.ovid.com/gw1/ovidweb.cgi (8 of 11)04.02.2007 00:22:00


hospital-free application. In conclusion, both ES and US can be used in cases of bone healing and delayed union.

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How to Obtain CME Category 1 Credits

To obtain CME Category 1 credit, this educational activity must be completed and postmarked by December 31, 1999. Participants may read the articles and take the exams

issue by issue or wait to study several issues together. After reading the three CME Articles in this issue, participants may complete the Self-Assessment Exam by answering the

questions on the CME Answering Sheet and the Evaluation pages, which appear later in this section. Send the completed forms to: CME Department, Association of Academic

Physiatrists, 5987 E. 71st Street, Suite 112, Indianapolis, IN 46220. Documentation can be received at the AAP National Office at any time throughout the year, and accurate

records will be maintained for each participant. CME certificates are issued only once a year in January for the total number of credits earned during the prior year.

Key Words: Bone Healing; Electrical Stimulation; Ultrasound; Nonunion; Delayed Union

Accession Number: 00002060-199809000-00013

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compmarative study of the effect of ultrasound and electrostimulation on bone healing in rats

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